diff --git a/src/commands/deploy/deploy.ts b/src/commands/deploy/deploy.ts
index 604874a9f..cf7b3e4d2 100644
--- a/src/commands/deploy/deploy.ts
+++ b/src/commands/deploy/deploy.ts
@@ -60,7 +60,7 @@ async function deploy(actionContext: IActionContext, arg1: vscode.Uri | string |
         expectedChildContextValue: expectedContextValue
     }));
 
-    const { language, version } = await verifyInitForVSCode(context, context.effectiveDeployFsPath);
+    const { language, languageModel, version } = await verifyInitForVSCode(context, context.effectiveDeployFsPath);
 
     context.telemetry.properties.projectLanguage = language;
     context.telemetry.properties.projectRuntime = version;
@@ -121,7 +121,16 @@ async function deploy(actionContext: IActionContext, arg1: vscode.Uri | string |
     }
 
     if (isZipDeploy) {
-        await verifyAppSettings(context, node, context.projectPath, version, language, { doRemoteBuild, isConsumption }, durableStorageType);
+        await verifyAppSettings({
+            context,
+            node,
+            projectPath: context.projectPath,
+            version,
+            language,
+            languageModel,
+            bools: { doRemoteBuild, isConsumption },
+            durableStorageType
+        });
     }
 
     await node.runWithTemporaryDescription(
diff --git a/src/commands/deploy/verifyAppSettings.ts b/src/commands/deploy/verifyAppSettings.ts
index fa4403ead..ec869a1b7 100644
--- a/src/commands/deploy/verifyAppSettings.ts
+++ b/src/commands/deploy/verifyAppSettings.ts
@@ -7,11 +7,12 @@ import type { StringDictionary } from '@azure/arm-appservice';
 import type { ParsedSite } from '@microsoft/vscode-azext-azureappservice';
 import { IActionContext } from '@microsoft/vscode-azext-utils';
 import * as vscode from 'vscode';
-import { ConnectionKey, ConnectionKeyValues, DurableBackend, DurableBackendValues, extensionVersionKey, ProjectLanguage, runFromPackageKey, workerRuntimeKey } from '../../constants';
+import { azureWebJobsFeatureFlags, ConnectionKey, ConnectionKeyValues, DurableBackend, DurableBackendValues, extensionVersionKey, ProjectLanguage, runFromPackageKey, workerRuntimeKey } from '../../constants';
 import { ext } from '../../extensionVariables';
 import { FuncVersion, tryParseFuncVersion } from '../../FuncVersion';
 import { localize } from '../../localize';
 import { SlotTreeItem } from '../../tree/SlotTreeItem';
+import { isNodeV4Plus, isPythonV2Plus } from '../../utils/programmingModelUtils';
 import { isKnownWorkerRuntime, promptToUpdateDotnetRuntime, tryGetFunctionsWorkerRuntimeForProject } from '../../vsCodeConfig/settings';
 import { ISetConnectionSettingContext } from '../appSettings/connectionSettings/ISetConnectionSettingContext';
 
@@ -20,7 +21,18 @@ import { ISetConnectionSettingContext } from '../appSettings/connectionSettings/
  */
 type VerifyAppSettingBooleans = { doRemoteBuild: boolean | undefined; isConsumption: boolean };
 
-export async function verifyAppSettings(context: IActionContext, node: SlotTreeItem, projectPath: string | undefined, version: FuncVersion, language: ProjectLanguage, bools: VerifyAppSettingBooleans, durableStorageType: DurableBackendValues | undefined): Promise<void> {
+export async function verifyAppSettings(options: {
+    context: IActionContext,
+    node: SlotTreeItem,
+    projectPath: string | undefined,
+    version: FuncVersion,
+    language: ProjectLanguage,
+    languageModel: number | undefined,
+    bools: VerifyAppSettingBooleans,
+    durableStorageType: DurableBackendValues | undefined
+}): Promise<void> {
+
+    const { context, node, projectPath, version, language, bools, durableStorageType } = options;
     const client = await node.site.createClient(context);
     const appSettings: StringDictionary = await client.listApplicationSettings();
     if (appSettings.properties) {
@@ -36,6 +48,10 @@ export async function verifyAppSettings(context: IActionContext, node: SlotTreeI
             updateAppSettings ||= verifyRunFromPackage(context, node.site, appSettings.properties);
         }
 
+        if (isNodeV4Plus(options) || isPythonV2Plus(options.language, options.languageModel)) {
+            updateAppSettings ||= verifyFeatureFlagSetting(context, node.site, appSettings.properties);
+        }
+
         const updatedRemoteConnection: boolean = await verifyAndUpdateAppConnectionStrings(context, durableStorageType, appSettings.properties);
         updateAppSettings ||= updatedRemoteConnection;
 
@@ -168,3 +184,21 @@ function verifyLinuxRemoteBuildSettings(context: IActionContext, remotePropertie
     return hasChanged;
 }
 
+function verifyFeatureFlagSetting(context: IActionContext, site: ParsedSite, remoteProperties: { [propertyName: string]: string }): boolean {
+    const featureFlagString = remoteProperties[azureWebJobsFeatureFlags] || '';
+
+    // Feature flags are comma-delimited lists of beta features
+    // https://learn.microsoft.com/en-us/azure/azure-functions/functions-app-settings#azurewebjobsfeatureflags
+    const featureFlagArray = !featureFlagString ? [] : featureFlagString.split(',');
+    const enableWorkerIndexingValue = 'EnableWorkerIndexing';
+    const shouldAddSetting: boolean = !featureFlagArray.includes(enableWorkerIndexingValue);
+
+    if (shouldAddSetting) {
+        featureFlagArray.push(enableWorkerIndexingValue);
+        ext.outputChannel.appendLog(localize('addedFeatureFlag', 'Added feature flag "{0}" because it is required for the new programming model', enableWorkerIndexingValue), { resourceName: site.fullName });
+        remoteProperties[azureWebJobsFeatureFlags] = featureFlagArray.join(',');
+    }
+
+    context.telemetry.properties.addedFeatureFlagSetting = String(shouldAddSetting);
+    return shouldAddSetting;
+}
diff --git a/src/constants.ts b/src/constants.ts
index a73267922..9d8037627 100644
--- a/src/constants.ts
+++ b/src/constants.ts
@@ -151,6 +151,7 @@ export const extensionVersionKey: string = 'FUNCTIONS_EXTENSION_VERSION';
 export const runFromPackageKey: string = 'WEBSITE_RUN_FROM_PACKAGE';
 export const contentConnectionStringKey: string = 'WEBSITE_CONTENTAZUREFILECONNECTIONSTRING';
 export const contentShareKey: string = 'WEBSITE_CONTENTSHARE';
+export const azureWebJobsFeatureFlags: string = 'AzureWebJobsFeatureFlags';
 
 /**
  * The "current" Node.js model is 3 (and assumed, if the number is omitted).