diff --git a/changelog.d/10844.feature b/changelog.d/10844.feature
new file mode 100644
index 000000000000..07e7b2c6a75e
--- /dev/null
+++ b/changelog.d/10844.feature
@@ -0,0 +1 @@
+Speed up responding with large JSON objects to requests.
diff --git a/synapse/http/server.py b/synapse/http/server.py
index b79fa722e931..0930f645fd12 100644
--- a/synapse/http/server.py
+++ b/synapse/http/server.py
@@ -21,7 +21,6 @@
 import urllib
 from http import HTTPStatus
 from inspect import isawaitable
-from io import BytesIO
 from typing import (
     Any,
     Awaitable,
@@ -37,7 +36,7 @@
 )
 
 import jinja2
-from canonicaljson import iterencode_canonical_json
+from canonicaljson import encode_canonical_json
 from typing_extensions import Protocol
 from zope.interface import implementer
 
@@ -45,7 +44,7 @@
 from twisted.python import failure
 from twisted.web import resource
 from twisted.web.server import NOT_DONE_YET, Request
-from twisted.web.static import File, NoRangeStaticProducer
+from twisted.web.static import File
 from twisted.web.util import redirectTo
 
 from synapse.api.errors import (
@@ -56,10 +55,11 @@
     UnrecognizedRequestError,
 )
 from synapse.http.site import SynapseRequest
-from synapse.logging.context import preserve_fn
+from synapse.logging.context import defer_to_thread, preserve_fn, run_in_background
 from synapse.logging.opentracing import trace_servlet
 from synapse.util import json_encoder
 from synapse.util.caches import intern_dict
+from synapse.util.iterutils import chunk_seq
 
 logger = logging.getLogger(__name__)
 
@@ -320,7 +320,7 @@ def __init__(self, canonical_json=False, extract_context=False):
 
     def _send_response(
         self,
-        request: Request,
+        request: SynapseRequest,
         code: int,
         response_object: Any,
     ):
@@ -620,16 +620,15 @@ def stopProducing(self) -> None:
         self._request = None
 
 
-def _encode_json_bytes(json_object: Any) -> Iterator[bytes]:
+def _encode_json_bytes(json_object: Any) -> bytes:
     """
     Encode an object into JSON. Returns an iterator of bytes.
     """
-    for chunk in json_encoder.iterencode(json_object):
-        yield chunk.encode("utf-8")
+    return json_encoder.encode(json_object).encode("utf-8")
 
 
 def respond_with_json(
-    request: Request,
+    request: SynapseRequest,
     code: int,
     json_object: Any,
     send_cors: bool = False,
@@ -659,7 +658,7 @@ def respond_with_json(
         return None
 
     if canonical_json:
-        encoder = iterencode_canonical_json
+        encoder = encode_canonical_json
     else:
         encoder = _encode_json_bytes
 
@@ -670,7 +669,9 @@ def respond_with_json(
     if send_cors:
         set_cors_headers(request)
 
-    _ByteProducer(request, encoder(json_object))
+    run_in_background(
+        _async_write_json_to_request_in_thread, request, encoder, json_object
+    )
     return NOT_DONE_YET
 
 
@@ -706,15 +707,35 @@ def respond_with_json_bytes(
     if send_cors:
         set_cors_headers(request)
 
-    # note that this is zero-copy (the bytesio shares a copy-on-write buffer with
-    # the original `bytes`).
-    bytes_io = BytesIO(json_bytes)
-
-    producer = NoRangeStaticProducer(request, bytes_io)
-    producer.start()
+    _write_json_bytes_to_request(request, json_bytes)
     return NOT_DONE_YET
 
 
+def _write_json_bytes_to_request(request: Request, json_bytes: bytes) -> None:
+    """Writes the JSON bytes to the request using an appropriate producer.
+
+    Note: This should be used instead of `Request.write` to correctly handle
+    large response bodies.
+    """
+
+    # The problem with dumping all of the json response into the `Request`
+    # object at once (via `Request.write`) is that doing so starts the timeout
+    # for the next request to be received: so if it takes longer than 60s to
+    # stream back the response to the client, the client never gets it.
+    #
+    # The correct solution is to use a Producer; then the timeout is only
+    # started once all of the content is sent over the TCP connection.
+
+    # To make sure we don't write the whole of the json at once we split it up
+    # into chunks.
+    chunk_size = 4096
+    bytes_generator = chunk_seq(json_bytes, chunk_size)
+
+    # We use a `_ByteProducer` here rather than `NoRangeStaticProducer` as the
+    # unit tests can't cope with being given a pull producer.
+    _ByteProducer(request, bytes_generator)
+
+
 def set_cors_headers(request: Request):
     """Set the CORS headers so that javascript running in a web browsers can
     use this API
@@ -809,3 +830,24 @@ def finish_request(request: Request):
         request.finish()
     except RuntimeError as e:
         logger.info("Connection disconnected before response was written: %r", e)
+
+
+async def _async_write_json_to_request_in_thread(
+    request: SynapseRequest,
+    json_encoder: Callable[[Any], bytes],
+    json_object: Any,
+):
+    """Encodes the given JSON object on a thread and then writes it to the
+    request.
+
+    This is done so that encoding large JSON objects doesn't block the reactor
+    thread.
+
+    Note: We don't use JsonEncoder.iterencode here as that falls back to the
+    Python implementation (rather than the C backend), which is *much* more
+    expensive.
+    """
+
+    json_str = await defer_to_thread(request.reactor, json_encoder, json_object)
+
+    _write_json_bytes_to_request(request, json_str)
diff --git a/synapse/http/site.py b/synapse/http/site.py
index c665a9d5db86..a22cd0a0b79a 100644
--- a/synapse/http/site.py
+++ b/synapse/http/site.py
@@ -14,14 +14,15 @@
 import contextlib
 import logging
 import time
-from typing import Optional, Tuple, Union
+from typing import Generator, Optional, Tuple, Union
 
 import attr
 from zope.interface import implementer
 
 from twisted.internet.interfaces import IAddress, IReactorTime
 from twisted.python.failure import Failure
-from twisted.web.resource import IResource
+from twisted.web.http import HTTPChannel
+from twisted.web.resource import IResource, Resource
 from twisted.web.server import Request, Site
 
 from synapse.config.server import ListenerConfig
@@ -61,10 +62,18 @@ class SynapseRequest(Request):
         logcontext: the log context for this request
     """
 
-    def __init__(self, channel, *args, max_request_body_size=1024, **kw):
-        Request.__init__(self, channel, *args, **kw)
+    def __init__(
+        self,
+        channel: HTTPChannel,
+        site: "SynapseSite",
+        *args,
+        max_request_body_size: int = 1024,
+        **kw,
+    ):
+        super().__init__(channel, *args, **kw)
         self._max_request_body_size = max_request_body_size
-        self.site: SynapseSite = channel.site
+        self.synapse_site = site
+        self.reactor = site.reactor
         self._channel = channel  # this is used by the tests
         self.start_time = 0.0
 
@@ -83,13 +92,13 @@ def __init__(self, channel, *args, max_request_body_size=1024, **kw):
         self._is_processing = False
 
         # the time when the asynchronous request handler completed its processing
-        self._processing_finished_time = None
+        self._processing_finished_time: Optional[float] = None
 
         # what time we finished sending the response to the client (or the connection
         # dropped)
-        self.finish_time = None
+        self.finish_time: Optional[float] = None
 
-    def __repr__(self):
+    def __repr__(self) -> str:
         # We overwrite this so that we don't log ``access_token``
         return "<%s at 0x%x method=%r uri=%r clientproto=%r site=%r>" % (
             self.__class__.__name__,
@@ -97,10 +106,10 @@ def __repr__(self):
             self.get_method(),
             self.get_redacted_uri(),
             self.clientproto.decode("ascii", errors="replace"),
-            self.site.site_tag,
+            self.synapse_site.site_tag,
         )
 
-    def handleContentChunk(self, data):
+    def handleContentChunk(self, data: bytes) -> None:
         # we should have a `content` by now.
         assert self.content, "handleContentChunk() called before gotLength()"
         if self.content.tell() + len(data) > self._max_request_body_size:
@@ -139,7 +148,7 @@ def requester(self, value: Union[Requester, str]) -> None:
         # If there's no authenticated entity, it was the requester.
         self.logcontext.request.authenticated_entity = authenticated_entity or requester
 
-    def get_request_id(self):
+    def get_request_id(self) -> str:
         return "%s-%i" % (self.get_method(), self.request_seq)
 
     def get_redacted_uri(self) -> str:
@@ -205,7 +214,7 @@ def get_authenticated_entity(self) -> Tuple[Optional[str], Optional[str]]:
 
         return None, None
 
-    def render(self, resrc):
+    def render(self, resrc: Resource) -> None:
         # this is called once a Resource has been found to serve the request; in our
         # case the Resource in question will normally be a JsonResource.
 
@@ -216,7 +225,7 @@ def render(self, resrc):
             request=ContextRequest(
                 request_id=request_id,
                 ip_address=self.getClientIP(),
-                site_tag=self.site.site_tag,
+                site_tag=self.synapse_site.site_tag,
                 # The requester is going to be unknown at this point.
                 requester=None,
                 authenticated_entity=None,
@@ -228,7 +237,7 @@ def render(self, resrc):
         )
 
         # override the Server header which is set by twisted
-        self.setHeader("Server", self.site.server_version_string)
+        self.setHeader("Server", self.synapse_site.server_version_string)
 
         with PreserveLoggingContext(self.logcontext):
             # we start the request metrics timer here with an initial stab
@@ -247,7 +256,7 @@ def render(self, resrc):
             requests_counter.labels(self.get_method(), self.request_metrics.name).inc()
 
     @contextlib.contextmanager
-    def processing(self):
+    def processing(self) -> Generator[None, None, None]:
         """Record the fact that we are processing this request.
 
         Returns a context manager; the correct way to use this is:
@@ -282,7 +291,7 @@ async def handle_request(request):
             if self.finish_time is not None:
                 self._finished_processing()
 
-    def finish(self):
+    def finish(self) -> None:
         """Called when all response data has been written to this Request.
 
         Overrides twisted.web.server.Request.finish to record the finish time and do
@@ -295,7 +304,7 @@ def finish(self):
             with PreserveLoggingContext(self.logcontext):
                 self._finished_processing()
 
-    def connectionLost(self, reason):
+    def connectionLost(self, reason: Union[Failure, Exception]) -> None:
         """Called when the client connection is closed before the response is written.
 
         Overrides twisted.web.server.Request.connectionLost to record the finish time and
@@ -327,7 +336,7 @@ def connectionLost(self, reason):
             if not self._is_processing:
                 self._finished_processing()
 
-    def _started_processing(self, servlet_name):
+    def _started_processing(self, servlet_name: str) -> None:
         """Record the fact that we are processing this request.
 
         This will log the request's arrival. Once the request completes,
@@ -346,17 +355,19 @@ def _started_processing(self, servlet_name):
             self.start_time, name=servlet_name, method=self.get_method()
         )
 
-        self.site.access_logger.debug(
+        self.synapse_site.access_logger.debug(
             "%s - %s - Received request: %s %s",
             self.getClientIP(),
-            self.site.site_tag,
+            self.synapse_site.site_tag,
             self.get_method(),
             self.get_redacted_uri(),
         )
 
-    def _finished_processing(self):
+    def _finished_processing(self) -> None:
         """Log the completion of this request and update the metrics"""
         assert self.logcontext is not None
+        assert self.finish_time is not None
+
         usage = self.logcontext.get_resource_usage()
 
         if self._processing_finished_time is None:
@@ -386,13 +397,13 @@ def _finished_processing(self):
         if authenticated_entity:
             requester = f"{authenticated_entity}|{requester}"
 
-        self.site.access_logger.log(
+        self.synapse_site.access_logger.log(
             log_level,
             "%s - %s - {%s}"
             " Processed request: %.3fsec/%.3fsec (%.3fsec, %.3fsec) (%.3fsec/%.3fsec/%d)"
             ' %sB %s "%s %s %s" "%s" [%d dbevts]',
             self.getClientIP(),
-            self.site.site_tag,
+            self.synapse_site.site_tag,
             requester,
             processing_time,
             response_send_time,
@@ -437,7 +448,7 @@ class XForwardedForRequest(SynapseRequest):
     _forwarded_for: "Optional[_XForwardedForAddress]" = None
     _forwarded_https: bool = False
 
-    def requestReceived(self, command, path, version):
+    def requestReceived(self, command: bytes, path: bytes, version: bytes) -> None:
         # this method is called by the Channel once the full request has been
         # received, to dispatch the request to a resource.
         # We can use it to set the IP address and protocol according to the
@@ -445,7 +456,7 @@ def requestReceived(self, command, path, version):
         self._process_forwarded_headers()
         return super().requestReceived(command, path, version)
 
-    def _process_forwarded_headers(self):
+    def _process_forwarded_headers(self) -> None:
         headers = self.requestHeaders.getRawHeaders(b"x-forwarded-for")
         if not headers:
             return
@@ -470,7 +481,7 @@ def _process_forwarded_headers(self):
             )
             self._forwarded_https = True
 
-    def isSecure(self):
+    def isSecure(self) -> bool:
         if self._forwarded_https:
             return True
         return super().isSecure()
@@ -520,7 +531,7 @@ def __init__(
         site_tag: str,
         config: ListenerConfig,
         resource: IResource,
-        server_version_string,
+        server_version_string: str,
         max_request_body_size: int,
         reactor: IReactorTime,
     ):
@@ -540,19 +551,23 @@ def __init__(
         Site.__init__(self, resource, reactor=reactor)
 
         self.site_tag = site_tag
+        self.reactor = reactor
 
         assert config.http_options is not None
         proxied = config.http_options.x_forwarded
         request_class = XForwardedForRequest if proxied else SynapseRequest
 
-        def request_factory(channel, queued) -> Request:
+        def request_factory(channel: HTTPChannel, queued: bool) -> Request:
             return request_class(
-                channel, max_request_body_size=max_request_body_size, queued=queued
+                channel,
+                self,
+                max_request_body_size=max_request_body_size,
+                queued=queued,
             )
 
         self.requestFactory = request_factory  # type: ignore
         self.access_logger = logging.getLogger(logger_name)
         self.server_version_string = server_version_string.encode("ascii")
 
-    def log(self, request):
+    def log(self, request: SynapseRequest) -> None:
         pass
diff --git a/synapse/push/emailpusher.py b/synapse/push/emailpusher.py
index e08e125cb8a5..cf5abdfbda49 100644
--- a/synapse/push/emailpusher.py
+++ b/synapse/push/emailpusher.py
@@ -184,7 +184,7 @@ async def _unsafe_process(self) -> None:
 
             should_notify_at = max(notif_ready_at, room_ready_at)
 
-            if should_notify_at < self.clock.time_msec():
+            if should_notify_at <= self.clock.time_msec():
                 # one of our notifications is ready for sending, so we send
                 # *one* email updating the user on their notifications,
                 # we then consider all previously outstanding notifications
diff --git a/synapse/rest/key/v2/remote_key_resource.py b/synapse/rest/key/v2/remote_key_resource.py
index d8fd7938a468..057ddc23dbfe 100644
--- a/synapse/rest/key/v2/remote_key_resource.py
+++ b/synapse/rest/key/v2/remote_key_resource.py
@@ -17,12 +17,11 @@
 
 from signedjson.sign import sign_json
 
-from twisted.web.server import Request
-
 from synapse.api.errors import Codes, SynapseError
 from synapse.crypto.keyring import ServerKeyFetcher
 from synapse.http.server import DirectServeJsonResource, respond_with_json
 from synapse.http.servlet import parse_integer, parse_json_object_from_request
+from synapse.http.site import SynapseRequest
 from synapse.types import JsonDict
 from synapse.util import json_decoder
 from synapse.util.async_helpers import yieldable_gather_results
@@ -100,7 +99,7 @@ def __init__(self, hs: "HomeServer"):
         self.federation_domain_whitelist = hs.config.federation_domain_whitelist
         self.config = hs.config
 
-    async def _async_render_GET(self, request: Request) -> None:
+    async def _async_render_GET(self, request: SynapseRequest) -> None:
         assert request.postpath is not None
         if len(request.postpath) == 1:
             (server,) = request.postpath
@@ -117,7 +116,7 @@ async def _async_render_GET(self, request: Request) -> None:
 
         await self.query_keys(request, query, query_remote_on_cache_miss=True)
 
-    async def _async_render_POST(self, request: Request) -> None:
+    async def _async_render_POST(self, request: SynapseRequest) -> None:
         content = parse_json_object_from_request(request)
 
         query = content["server_keys"]
@@ -126,7 +125,7 @@ async def _async_render_POST(self, request: Request) -> None:
 
     async def query_keys(
         self,
-        request: Request,
+        request: SynapseRequest,
         query: JsonDict,
         query_remote_on_cache_miss: bool = False,
     ) -> None:
diff --git a/synapse/rest/media/v1/_base.py b/synapse/rest/media/v1/_base.py
index 7c881f2bdb18..014fa893d6c8 100644
--- a/synapse/rest/media/v1/_base.py
+++ b/synapse/rest/media/v1/_base.py
@@ -27,6 +27,7 @@
 
 from synapse.api.errors import Codes, SynapseError, cs_error
 from synapse.http.server import finish_request, respond_with_json
+from synapse.http.site import SynapseRequest
 from synapse.logging.context import make_deferred_yieldable
 from synapse.util.stringutils import is_ascii
 
@@ -74,7 +75,7 @@ def parse_media_id(request: Request) -> Tuple[str, str, Optional[str]]:
         )
 
 
-def respond_404(request: Request) -> None:
+def respond_404(request: SynapseRequest) -> None:
     respond_with_json(
         request,
         404,
@@ -84,7 +85,7 @@ def respond_404(request: Request) -> None:
 
 
 async def respond_with_file(
-    request: Request,
+    request: SynapseRequest,
     media_type: str,
     file_path: str,
     file_size: Optional[int] = None,
@@ -221,7 +222,7 @@ def _can_encode_filename_as_token(x: str) -> bool:
 
 
 async def respond_with_responder(
-    request: Request,
+    request: SynapseRequest,
     responder: "Optional[Responder]",
     media_type: str,
     file_size: Optional[int],
diff --git a/synapse/rest/media/v1/config_resource.py b/synapse/rest/media/v1/config_resource.py
index a1d36e5cf189..712d4e83681a 100644
--- a/synapse/rest/media/v1/config_resource.py
+++ b/synapse/rest/media/v1/config_resource.py
@@ -16,8 +16,6 @@
 
 from typing import TYPE_CHECKING
 
-from twisted.web.server import Request
-
 from synapse.http.server import DirectServeJsonResource, respond_with_json
 from synapse.http.site import SynapseRequest
 
@@ -39,5 +37,5 @@ async def _async_render_GET(self, request: SynapseRequest) -> None:
         await self.auth.get_user_by_req(request)
         respond_with_json(request, 200, self.limits_dict, send_cors=True)
 
-    async def _async_render_OPTIONS(self, request: Request) -> None:
+    async def _async_render_OPTIONS(self, request: SynapseRequest) -> None:
         respond_with_json(request, 200, {}, send_cors=True)
diff --git a/synapse/rest/media/v1/download_resource.py b/synapse/rest/media/v1/download_resource.py
index d6d938953e44..6180fa575ebc 100644
--- a/synapse/rest/media/v1/download_resource.py
+++ b/synapse/rest/media/v1/download_resource.py
@@ -15,10 +15,9 @@
 import logging
 from typing import TYPE_CHECKING
 
-from twisted.web.server import Request
-
 from synapse.http.server import DirectServeJsonResource, set_cors_headers
 from synapse.http.servlet import parse_boolean
+from synapse.http.site import SynapseRequest
 
 from ._base import parse_media_id, respond_404
 
@@ -37,7 +36,7 @@ def __init__(self, hs: "HomeServer", media_repo: "MediaRepository"):
         self.media_repo = media_repo
         self.server_name = hs.hostname
 
-    async def _async_render_GET(self, request: Request) -> None:
+    async def _async_render_GET(self, request: SynapseRequest) -> None:
         set_cors_headers(request)
         request.setHeader(
             b"Content-Security-Policy",
diff --git a/synapse/rest/media/v1/media_repository.py b/synapse/rest/media/v1/media_repository.py
index 50e4c9e29f26..28fa3c72e4d9 100644
--- a/synapse/rest/media/v1/media_repository.py
+++ b/synapse/rest/media/v1/media_repository.py
@@ -23,7 +23,6 @@
 import twisted.web.http
 from twisted.internet.defer import Deferred
 from twisted.web.resource import Resource
-from twisted.web.server import Request
 
 from synapse.api.errors import (
     FederationDeniedError,
@@ -34,6 +33,7 @@
 )
 from synapse.config._base import ConfigError
 from synapse.config.repository import ThumbnailRequirement
+from synapse.http.site import SynapseRequest
 from synapse.logging.context import defer_to_thread
 from synapse.metrics.background_process_metrics import run_as_background_process
 from synapse.types import UserID
@@ -187,7 +187,7 @@ async def create_content(
         return "mxc://%s/%s" % (self.server_name, media_id)
 
     async def get_local_media(
-        self, request: Request, media_id: str, name: Optional[str]
+        self, request: SynapseRequest, media_id: str, name: Optional[str]
     ) -> None:
         """Responds to requests for local media, if exists, or returns 404.
 
@@ -221,7 +221,11 @@ async def get_local_media(
         )
 
     async def get_remote_media(
-        self, request: Request, server_name: str, media_id: str, name: Optional[str]
+        self,
+        request: SynapseRequest,
+        server_name: str,
+        media_id: str,
+        name: Optional[str],
     ) -> None:
         """Respond to requests for remote media.
 
diff --git a/synapse/rest/media/v1/preview_url_resource.py b/synapse/rest/media/v1/preview_url_resource.py
index fe0627d9b0e6..16f16b482092 100644
--- a/synapse/rest/media/v1/preview_url_resource.py
+++ b/synapse/rest/media/v1/preview_url_resource.py
@@ -29,7 +29,6 @@
 
 from twisted.internet.defer import Deferred
 from twisted.internet.error import DNSLookupError
-from twisted.web.server import Request
 
 from synapse.api.errors import Codes, SynapseError
 from synapse.http.client import SimpleHttpClient
@@ -167,7 +166,7 @@ def __init__(
                 self._start_expire_url_cache_data, 10 * 1000
             )
 
-    async def _async_render_OPTIONS(self, request: Request) -> None:
+    async def _async_render_OPTIONS(self, request: SynapseRequest) -> None:
         request.setHeader(b"Allow", b"OPTIONS, GET")
         respond_with_json(request, 200, {}, send_cors=True)
 
diff --git a/synapse/rest/media/v1/thumbnail_resource.py b/synapse/rest/media/v1/thumbnail_resource.py
index 22f43d85310b..cb2f88676ec1 100644
--- a/synapse/rest/media/v1/thumbnail_resource.py
+++ b/synapse/rest/media/v1/thumbnail_resource.py
@@ -17,11 +17,10 @@
 import logging
 from typing import TYPE_CHECKING, Any, Dict, List, Optional, Tuple
 
-from twisted.web.server import Request
-
 from synapse.api.errors import SynapseError
 from synapse.http.server import DirectServeJsonResource, set_cors_headers
 from synapse.http.servlet import parse_integer, parse_string
+from synapse.http.site import SynapseRequest
 from synapse.rest.media.v1.media_storage import MediaStorage
 
 from ._base import (
@@ -57,7 +56,7 @@ def __init__(
         self.dynamic_thumbnails = hs.config.dynamic_thumbnails
         self.server_name = hs.hostname
 
-    async def _async_render_GET(self, request: Request) -> None:
+    async def _async_render_GET(self, request: SynapseRequest) -> None:
         set_cors_headers(request)
         server_name, media_id, _ = parse_media_id(request)
         width = parse_integer(request, "width", required=True)
@@ -88,7 +87,7 @@ async def _async_render_GET(self, request: Request) -> None:
 
     async def _respond_local_thumbnail(
         self,
-        request: Request,
+        request: SynapseRequest,
         media_id: str,
         width: int,
         height: int,
@@ -121,7 +120,7 @@ async def _respond_local_thumbnail(
 
     async def _select_or_generate_local_thumbnail(
         self,
-        request: Request,
+        request: SynapseRequest,
         media_id: str,
         desired_width: int,
         desired_height: int,
@@ -186,7 +185,7 @@ async def _select_or_generate_local_thumbnail(
 
     async def _select_or_generate_remote_thumbnail(
         self,
-        request: Request,
+        request: SynapseRequest,
         server_name: str,
         media_id: str,
         desired_width: int,
@@ -249,7 +248,7 @@ async def _select_or_generate_remote_thumbnail(
 
     async def _respond_remote_thumbnail(
         self,
-        request: Request,
+        request: SynapseRequest,
         server_name: str,
         media_id: str,
         width: int,
@@ -280,7 +279,7 @@ async def _respond_remote_thumbnail(
 
     async def _select_and_respond_with_thumbnail(
         self,
-        request: Request,
+        request: SynapseRequest,
         desired_width: int,
         desired_height: int,
         desired_method: str,
diff --git a/synapse/rest/media/v1/upload_resource.py b/synapse/rest/media/v1/upload_resource.py
index 146adca8f1bf..39b29318bbe8 100644
--- a/synapse/rest/media/v1/upload_resource.py
+++ b/synapse/rest/media/v1/upload_resource.py
@@ -16,8 +16,6 @@
 import logging
 from typing import IO, TYPE_CHECKING, Dict, List, Optional
 
-from twisted.web.server import Request
-
 from synapse.api.errors import Codes, SynapseError
 from synapse.http.server import DirectServeJsonResource, respond_with_json
 from synapse.http.servlet import parse_bytes_from_args
@@ -46,7 +44,7 @@ def __init__(self, hs: "HomeServer", media_repo: "MediaRepository"):
         self.max_upload_size = hs.config.max_upload_size
         self.clock = hs.get_clock()
 
-    async def _async_render_OPTIONS(self, request: Request) -> None:
+    async def _async_render_OPTIONS(self, request: SynapseRequest) -> None:
         respond_with_json(request, 200, {}, send_cors=True)
 
     async def _async_render_POST(self, request: SynapseRequest) -> None:
diff --git a/synapse/util/iterutils.py b/synapse/util/iterutils.py
index 8ac3eab2f54f..4938ddf70321 100644
--- a/synapse/util/iterutils.py
+++ b/synapse/util/iterutils.py
@@ -21,13 +21,28 @@
     Iterable,
     Iterator,
     Mapping,
-    Sequence,
     Set,
+    Sized,
     Tuple,
     TypeVar,
 )
 
+from typing_extensions import Protocol
+
 T = TypeVar("T")
+S = TypeVar("S", bound="_SelfSlice")
+
+
+class _SelfSlice(Sized, Protocol):
+    """A helper protocol that matches types where taking a slice results in the
+    same type being returned.
+
+    This is more specific than `Sequence`, which allows another `Sequence` to be
+    returned.
+    """
+
+    def __getitem__(self: S, i: slice) -> S:
+        ...
 
 
 def batch_iter(iterable: Iterable[T], size: int) -> Iterator[Tuple[T, ...]]:
@@ -46,7 +61,7 @@ def batch_iter(iterable: Iterable[T], size: int) -> Iterator[Tuple[T, ...]]:
     return iter(lambda: tuple(islice(sourceiter, size)), ())
 
 
-def chunk_seq(iseq: Sequence[T], maxlen: int) -> Iterable[Sequence[T]]:
+def chunk_seq(iseq: S, maxlen: int) -> Iterator[S]:
     """Split the given sequence into chunks of the given size
 
     The last chunk may be shorter than the given size.
diff --git a/tests/http/test_additional_resource.py b/tests/http/test_additional_resource.py
index 768c2ba4ead3..391196425c38 100644
--- a/tests/http/test_additional_resource.py
+++ b/tests/http/test_additional_resource.py
@@ -45,7 +45,9 @@ def test_async(self):
         handler = _AsyncTestCustomEndpoint({}, None).handle_request
         resource = AdditionalResource(self.hs, handler)
 
-        channel = make_request(self.reactor, FakeSite(resource), "GET", "/")
+        channel = make_request(
+            self.reactor, FakeSite(resource, self.reactor), "GET", "/"
+        )
 
         self.assertEqual(channel.code, 200)
         self.assertEqual(channel.json_body, {"some_key": "some_value_async"})
@@ -54,7 +56,9 @@ def test_sync(self):
         handler = _SyncTestCustomEndpoint({}, None).handle_request
         resource = AdditionalResource(self.hs, handler)
 
-        channel = make_request(self.reactor, FakeSite(resource), "GET", "/")
+        channel = make_request(
+            self.reactor, FakeSite(resource, self.reactor), "GET", "/"
+        )
 
         self.assertEqual(channel.code, 200)
         self.assertEqual(channel.json_body, {"some_key": "some_value_sync"})
diff --git a/tests/logging/test_terse_json.py b/tests/logging/test_terse_json.py
index 116071692976..f73fcd684e0e 100644
--- a/tests/logging/test_terse_json.py
+++ b/tests/logging/test_terse_json.py
@@ -152,7 +152,8 @@ def test_with_request_context(self):
         site = Mock(spec=["site_tag", "server_version_string", "getResourceFor"])
         site.site_tag = "test-site"
         site.server_version_string = "Server v1"
-        request = SynapseRequest(FakeChannel(site, None))
+        site.reactor = Mock()
+        request = SynapseRequest(FakeChannel(site, None), site)
         # Call requestReceived to finish instantiating the object.
         request.content = BytesIO()
         # Partially skip some of the internal processing of SynapseRequest.
diff --git a/tests/replication/test_multi_media_repo.py b/tests/replication/test_multi_media_repo.py
index 01b1b0d4a002..13aa5eb51aa5 100644
--- a/tests/replication/test_multi_media_repo.py
+++ b/tests/replication/test_multi_media_repo.py
@@ -68,7 +68,7 @@ def _get_media_req(
         resource = hs.get_media_repository_resource().children[b"download"]
         channel = make_request(
             self.reactor,
-            FakeSite(resource),
+            FakeSite(resource, self.reactor),
             "GET",
             f"/{target}/{media_id}",
             shorthand=False,
diff --git a/tests/rest/admin/test_admin.py b/tests/rest/admin/test_admin.py
index febd40b65609..192073c5203f 100644
--- a/tests/rest/admin/test_admin.py
+++ b/tests/rest/admin/test_admin.py
@@ -201,7 +201,7 @@ def _ensure_quarantined(self, admin_user_tok, server_and_media_id):
         """Ensure a piece of media is quarantined when trying to access it."""
         channel = make_request(
             self.reactor,
-            FakeSite(self.download_resource),
+            FakeSite(self.download_resource, self.reactor),
             "GET",
             server_and_media_id,
             shorthand=False,
@@ -271,7 +271,7 @@ def test_quarantine_media_by_id(self):
         # Attempt to access the media
         channel = make_request(
             self.reactor,
-            FakeSite(self.download_resource),
+            FakeSite(self.download_resource, self.reactor),
             "GET",
             server_name_and_media_id,
             shorthand=False,
@@ -458,7 +458,7 @@ def test_cannot_quarantine_safe_media(self):
         # Attempt to access each piece of media
         channel = make_request(
             self.reactor,
-            FakeSite(self.download_resource),
+            FakeSite(self.download_resource, self.reactor),
             "GET",
             server_and_media_id_2,
             shorthand=False,
diff --git a/tests/rest/admin/test_media.py b/tests/rest/admin/test_media.py
index 2f02934e72b1..f8138660736b 100644
--- a/tests/rest/admin/test_media.py
+++ b/tests/rest/admin/test_media.py
@@ -125,7 +125,7 @@ def test_delete_media(self):
         # Attempt to access media
         channel = make_request(
             self.reactor,
-            FakeSite(download_resource),
+            FakeSite(download_resource, self.reactor),
             "GET",
             server_and_media_id,
             shorthand=False,
@@ -164,7 +164,7 @@ def test_delete_media(self):
         # Attempt to access media
         channel = make_request(
             self.reactor,
-            FakeSite(download_resource),
+            FakeSite(download_resource, self.reactor),
             "GET",
             server_and_media_id,
             shorthand=False,
@@ -525,7 +525,7 @@ def _access_media(self, server_and_media_id, expect_success=True):
 
         channel = make_request(
             self.reactor,
-            FakeSite(download_resource),
+            FakeSite(download_resource, self.reactor),
             "GET",
             server_and_media_id,
             shorthand=False,
diff --git a/tests/rest/admin/test_user.py b/tests/rest/admin/test_user.py
index cc3f16c62ae5..e79e0e1850b8 100644
--- a/tests/rest/admin/test_user.py
+++ b/tests/rest/admin/test_user.py
@@ -2973,7 +2973,7 @@ def _create_media_and_access(
         # Try to access a media and to create `last_access_ts`
         channel = make_request(
             self.reactor,
-            FakeSite(download_resource),
+            FakeSite(download_resource, self.reactor),
             "GET",
             server_and_media_id,
             shorthand=False,
diff --git a/tests/rest/client/test_account.py b/tests/rest/client/test_account.py
index b946fca8b367..9e9e953cf4b2 100644
--- a/tests/rest/client/test_account.py
+++ b/tests/rest/client/test_account.py
@@ -312,7 +312,7 @@ def _validate_token(self, link):
         # Load the password reset confirmation page
         channel = make_request(
             self.reactor,
-            FakeSite(self.submit_token_resource),
+            FakeSite(self.submit_token_resource, self.reactor),
             "GET",
             path,
             shorthand=False,
@@ -326,7 +326,7 @@ def _validate_token(self, link):
         # Confirm the password reset
         channel = make_request(
             self.reactor,
-            FakeSite(self.submit_token_resource),
+            FakeSite(self.submit_token_resource, self.reactor),
             "POST",
             path,
             content=b"",
diff --git a/tests/rest/client/test_consent.py b/tests/rest/client/test_consent.py
index 65c58ce70a84..84d092ca8242 100644
--- a/tests/rest/client/test_consent.py
+++ b/tests/rest/client/test_consent.py
@@ -61,7 +61,11 @@ def test_render_public_consent(self):
         """You can observe the terms form without specifying a user"""
         resource = consent_resource.ConsentResource(self.hs)
         channel = make_request(
-            self.reactor, FakeSite(resource), "GET", "/consent?v=1", shorthand=False
+            self.reactor,
+            FakeSite(resource, self.reactor),
+            "GET",
+            "/consent?v=1",
+            shorthand=False,
         )
         self.assertEqual(channel.code, 200)
 
@@ -83,7 +87,7 @@ def test_accept_consent(self):
         )
         channel = make_request(
             self.reactor,
-            FakeSite(resource),
+            FakeSite(resource, self.reactor),
             "GET",
             consent_uri,
             access_token=access_token,
@@ -98,7 +102,7 @@ def test_accept_consent(self):
         # POST to the consent page, saying we've agreed
         channel = make_request(
             self.reactor,
-            FakeSite(resource),
+            FakeSite(resource, self.reactor),
             "POST",
             consent_uri + "&v=" + version,
             access_token=access_token,
@@ -110,7 +114,7 @@ def test_accept_consent(self):
         # changed
         channel = make_request(
             self.reactor,
-            FakeSite(resource),
+            FakeSite(resource, self.reactor),
             "GET",
             consent_uri,
             access_token=access_token,
diff --git a/tests/rest/client/utils.py b/tests/rest/client/utils.py
index 954ad1a1fdef..e55936d9c3bd 100644
--- a/tests/rest/client/utils.py
+++ b/tests/rest/client/utils.py
@@ -372,7 +372,7 @@ def upload_media(
         path = "/_matrix/media/r0/upload?filename=%s" % (filename,)
         channel = make_request(
             self.hs.get_reactor(),
-            FakeSite(resource),
+            FakeSite(resource, self.hs.get_reactor()),
             "POST",
             path,
             content=image_data,
diff --git a/tests/rest/key/v2/test_remote_key_resource.py b/tests/rest/key/v2/test_remote_key_resource.py
index a75c0ea3f04a..4672a6859684 100644
--- a/tests/rest/key/v2/test_remote_key_resource.py
+++ b/tests/rest/key/v2/test_remote_key_resource.py
@@ -84,7 +84,7 @@ def make_notary_request(self, server_name: str, key_id: str) -> dict:
         Checks that the response is a 200 and returns the decoded json body.
         """
         channel = FakeChannel(self.site, self.reactor)
-        req = SynapseRequest(channel)
+        req = SynapseRequest(channel, self.site)
         req.content = BytesIO(b"")
         req.requestReceived(
             b"GET",
@@ -183,7 +183,7 @@ async def post_json(destination, path, data):
             )
 
             channel = FakeChannel(self.site, self.reactor)
-            req = SynapseRequest(channel)
+            req = SynapseRequest(channel, self.site)
             req.content = BytesIO(encode_canonical_json(data))
 
             req.requestReceived(
diff --git a/tests/rest/media/v1/test_media_storage.py b/tests/rest/media/v1/test_media_storage.py
index 9ea1c2bf25c1..44a643d50613 100644
--- a/tests/rest/media/v1/test_media_storage.py
+++ b/tests/rest/media/v1/test_media_storage.py
@@ -252,7 +252,7 @@ def _req(self, content_disposition):
 
         channel = make_request(
             self.reactor,
-            FakeSite(self.download_resource),
+            FakeSite(self.download_resource, self.reactor),
             "GET",
             self.media_id,
             shorthand=False,
@@ -384,7 +384,7 @@ def test_thumbnail_repeated_thumbnail(self):
         params = "?width=32&height=32&method=scale"
         channel = make_request(
             self.reactor,
-            FakeSite(self.thumbnail_resource),
+            FakeSite(self.thumbnail_resource, self.reactor),
             "GET",
             self.media_id + params,
             shorthand=False,
@@ -413,7 +413,7 @@ def test_thumbnail_repeated_thumbnail(self):
 
         channel = make_request(
             self.reactor,
-            FakeSite(self.thumbnail_resource),
+            FakeSite(self.thumbnail_resource, self.reactor),
             "GET",
             self.media_id + params,
             shorthand=False,
@@ -433,7 +433,7 @@ def _test_thumbnail(self, method, expected_body, expected_found):
         params = "?width=32&height=32&method=" + method
         channel = make_request(
             self.reactor,
-            FakeSite(self.thumbnail_resource),
+            FakeSite(self.thumbnail_resource, self.reactor),
             "GET",
             self.media_id + params,
             shorthand=False,
diff --git a/tests/server.py b/tests/server.py
index b861c7b866f8..88dfa8058e62 100644
--- a/tests/server.py
+++ b/tests/server.py
@@ -19,6 +19,7 @@
     IPullProducer,
     IPushProducer,
     IReactorPluggableNameResolver,
+    IReactorTime,
     IResolverSimple,
     ITransport,
 )
@@ -181,13 +182,14 @@ class FakeSite:
     site_tag = "test"
     access_logger = logging.getLogger("synapse.access.http.fake")
 
-    def __init__(self, resource: IResource):
+    def __init__(self, resource: IResource, reactor: IReactorTime):
         """
 
         Args:
             resource: the resource to be used for rendering all requests
         """
         self._resource = resource
+        self.reactor = reactor
 
     def getResourceFor(self, request):
         return self._resource
@@ -268,7 +270,7 @@ def make_request(
 
     channel = FakeChannel(site, reactor, ip=client_ip)
 
-    req = request(channel)
+    req = request(channel, site)
     req.content = BytesIO(content)
     # Twisted expects to be at the end of the content when parsing the request.
     req.content.seek(SEEK_END)
diff --git a/tests/test_server.py b/tests/test_server.py
index 407e172e41de..f2ffbc895b88 100644
--- a/tests/test_server.py
+++ b/tests/test_server.py
@@ -65,7 +65,10 @@ def _callback(request, **kwargs):
         )
 
         make_request(
-            self.reactor, FakeSite(res), b"GET", b"/_matrix/foo/%E2%98%83?a=%E2%98%83"
+            self.reactor,
+            FakeSite(res, self.reactor),
+            b"GET",
+            b"/_matrix/foo/%E2%98%83?a=%E2%98%83",
         )
 
         self.assertEqual(got_kwargs, {"room_id": "\N{SNOWMAN}"})
@@ -84,7 +87,9 @@ def _callback(request, **kwargs):
             "GET", [re.compile("^/_matrix/foo$")], _callback, "test_servlet"
         )
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/_matrix/foo")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/_matrix/foo"
+        )
 
         self.assertEqual(channel.result["code"], b"500")
 
@@ -100,7 +105,7 @@ def _throw(*args):
         def _callback(request, **kwargs):
             d = Deferred()
             d.addCallback(_throw)
-            self.reactor.callLater(1, d.callback, True)
+            self.reactor.callLater(0.5, d.callback, True)
             return make_deferred_yieldable(d)
 
         res = JsonResource(self.homeserver)
@@ -108,7 +113,9 @@ def _callback(request, **kwargs):
             "GET", [re.compile("^/_matrix/foo$")], _callback, "test_servlet"
         )
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/_matrix/foo")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/_matrix/foo"
+        )
 
         self.assertEqual(channel.result["code"], b"500")
 
@@ -126,7 +133,9 @@ def _callback(request, **kwargs):
             "GET", [re.compile("^/_matrix/foo$")], _callback, "test_servlet"
         )
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/_matrix/foo")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/_matrix/foo"
+        )
 
         self.assertEqual(channel.result["code"], b"403")
         self.assertEqual(channel.json_body["error"], "Forbidden!!one!")
@@ -148,7 +157,9 @@ def _callback(request, **kwargs):
             "GET", [re.compile("^/_matrix/foo$")], _callback, "test_servlet"
         )
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/_matrix/foobar")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/_matrix/foobar"
+        )
 
         self.assertEqual(channel.result["code"], b"400")
         self.assertEqual(channel.json_body["error"], "Unrecognized request")
@@ -173,7 +184,9 @@ def _callback(request, **kwargs):
         )
 
         # The path was registered as GET, but this is a HEAD request.
-        channel = make_request(self.reactor, FakeSite(res), b"HEAD", b"/_matrix/foo")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"HEAD", b"/_matrix/foo"
+        )
 
         self.assertEqual(channel.result["code"], b"200")
         self.assertNotIn("body", channel.result)
@@ -280,7 +293,9 @@ async def callback(request):
         res = WrapHtmlRequestHandlerTests.TestResource()
         res.callback = callback
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/path")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/path"
+        )
 
         self.assertEqual(channel.result["code"], b"200")
         body = channel.result["body"]
@@ -298,7 +313,9 @@ async def callback(request, **kwargs):
         res = WrapHtmlRequestHandlerTests.TestResource()
         res.callback = callback
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/path")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/path"
+        )
 
         self.assertEqual(channel.result["code"], b"301")
         headers = channel.result["headers"]
@@ -319,7 +336,9 @@ async def callback(request, **kwargs):
         res = WrapHtmlRequestHandlerTests.TestResource()
         res.callback = callback
 
-        channel = make_request(self.reactor, FakeSite(res), b"GET", b"/path")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"GET", b"/path"
+        )
 
         self.assertEqual(channel.result["code"], b"304")
         headers = channel.result["headers"]
@@ -338,7 +357,9 @@ async def callback(request):
         res = WrapHtmlRequestHandlerTests.TestResource()
         res.callback = callback
 
-        channel = make_request(self.reactor, FakeSite(res), b"HEAD", b"/path")
+        channel = make_request(
+            self.reactor, FakeSite(res, self.reactor), b"HEAD", b"/path"
+        )
 
         self.assertEqual(channel.result["code"], b"200")
         self.assertNotIn("body", channel.result)