diff --git a/lib/active_model/serializer/collection_serializer.rb b/lib/active_model/serializer/collection_serializer.rb
index a3c9dc476..6f568953a 100644
--- a/lib/active_model/serializer/collection_serializer.rb
+++ b/lib/active_model/serializer/collection_serializer.rb
@@ -23,8 +23,11 @@ def initialize(resources, options = {})
       end
 
       def json_key
-        key = root || serializers.first.try(:json_key) || object.try(:name).try(:underscore)
-        key.try(:pluralize)
+        root || begin
+          singular_key = serializers.first.try(:json_key) ||
+            object.try(:name).try(:underscore)
+          singular_key.try(:pluralize)
+        end
       end
 
       def paginated?
diff --git a/test/action_controller/serialization_test.rb b/test/action_controller/serialization_test.rb
index a3b761981..d2fe3959e 100644
--- a/test/action_controller/serialization_test.rb
+++ b/test/action_controller/serialization_test.rb
@@ -171,7 +171,7 @@ def test_render_array_using_custom_root
         with_adapter :json do
           get :render_array_using_custom_root
         end
-        expected = { custom_roots: [{ name: 'Name 1', description: 'Description 1' }] }
+        expected = { custom_root: [{ name: 'Name 1', description: 'Description 1' }] }
         assert_equal 'application/json', @response.content_type
         assert_equal expected.to_json, @response.body
       end
@@ -181,7 +181,7 @@ def test_render_array_that_is_empty_using_custom_root
           get :render_array_that_is_empty_using_custom_root
         end
 
-        expected = { custom_roots: [] }
+        expected = { custom_root: [] }
         assert_equal 'application/json', @response.content_type
         assert_equal expected.to_json, @response.body
       end
diff --git a/test/collection_serializer_test.rb b/test/collection_serializer_test.rb
index 662aa1ee4..a7c0fa021 100644
--- a/test/collection_serializer_test.rb
+++ b/test/collection_serializer_test.rb
@@ -62,8 +62,9 @@ def test_root_with_no_serializers
         assert_equal expected, @serializer.root
       end
 
-      def test_json_key
-        assert_equal 'comments', @serializer.json_key
+      def test_json_key_with_resource_with_serializer
+        singular_key = @serializer.send(:serializers).first.json_key
+        assert_equal singular_key.pluralize, @serializer.json_key
       end
 
       def test_json_key_with_resource_with_name_and_no_serializers
@@ -84,13 +85,15 @@ def test_json_key_with_resource_without_name_and_no_serializers
       end
 
       def test_json_key_with_root
-        serializer = collection_serializer.new(@resource, root: 'custom_root')
-        assert_equal 'custom_roots', serializer.json_key
+        expected = 'custom_root'
+        serializer = collection_serializer.new(@resource, root: expected)
+        assert_equal expected, serializer.json_key
       end
 
       def test_json_key_with_root_and_no_serializers
-        serializer = collection_serializer.new(build_named_collection, root: 'custom_root')
-        assert_equal 'custom_roots', serializer.json_key
+        expected = 'custom_root'
+        serializer = collection_serializer.new(build_named_collection, root: expected)
+        assert_equal expected, serializer.json_key
       end
     end
   end