diff --git a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-create.ts b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-create.ts
index e1d612e54bc..bffec8887ed 100644
--- a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-create.ts
+++ b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-create.ts
@@ -7,6 +7,7 @@ import {TypedDocumentNode as DocumentNode} from '@graphql-typed-document-node/co
 export type DevSessionCreateMutationVariables = Types.Exact<{
   appId: Types.Scalars['String']['input']
   assetsUrl: Types.Scalars['String']['input']
+  websocketUrl?: Types.InputMaybe<Types.Scalars['String']['input']>
 }>
 
 export type DevSessionCreateMutation = {
@@ -15,7 +16,7 @@ export type DevSessionCreateMutation = {
   } | null
 }
 
-export const DevSessionCreate = {
+export const DevSessionCreateDocument = {
   kind: 'Document',
   definitions: [
     {
@@ -33,6 +34,11 @@ export const DevSessionCreate = {
           variable: {kind: 'Variable', name: {kind: 'Name', value: 'assetsUrl'}},
           type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
         },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'websocketUrl'}},
+          type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}},
+        },
       ],
       selectionSet: {
         kind: 'SelectionSet',
@@ -51,6 +57,11 @@ export const DevSessionCreate = {
                 name: {kind: 'Name', value: 'assetsUrl'},
                 value: {kind: 'Variable', name: {kind: 'Name', value: 'assetsUrl'}},
               },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'websocketUrl'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'websocketUrl'}},
+              },
             ],
             selectionSet: {
               kind: 'SelectionSet',
diff --git a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-delete.ts b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-delete.ts
index 3f6ccb87cae..f4ee5554fb8 100644
--- a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-delete.ts
+++ b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-delete.ts
@@ -9,7 +9,7 @@ export type DevSessionDeleteMutationVariables = Types.Exact<{
 
 export type DevSessionDeleteMutation = {devSessionDelete?: {userErrors: {message: string}[]} | null}
 
-export const DevSessionDelete = {
+export const DevSessionDeleteDocument = {
   kind: 'Document',
   definitions: [
     {
diff --git a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-update.ts b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-update.ts
index 243629fa441..142fae8b5b0 100644
--- a/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-update.ts
+++ b/packages/app/src/cli/api/graphql/app-dev/generated/dev-session-update.ts
@@ -7,6 +7,7 @@ import {TypedDocumentNode as DocumentNode} from '@graphql-typed-document-node/co
 export type DevSessionUpdateMutationVariables = Types.Exact<{
   appId: Types.Scalars['String']['input']
   assetsUrl?: Types.InputMaybe<Types.Scalars['String']['input']>
+  websocketUrl?: Types.InputMaybe<Types.Scalars['String']['input']>
   manifest?: Types.InputMaybe<Types.Scalars['JSON']['input']>
   inheritedModuleUids: Types.Scalars['String']['input'][] | Types.Scalars['String']['input']
 }>
@@ -17,7 +18,7 @@ export type DevSessionUpdateMutation = {
   } | null
 }
 
-export const DevSessionUpdate = {
+export const DevSessionUpdateDocument = {
   kind: 'Document',
   definitions: [
     {
@@ -35,6 +36,11 @@ export const DevSessionUpdate = {
           variable: {kind: 'Variable', name: {kind: 'Name', value: 'assetsUrl'}},
           type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}},
         },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'websocketUrl'}},
+          type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}},
+        },
         {
           kind: 'VariableDefinition',
           variable: {kind: 'Variable', name: {kind: 'Name', value: 'manifest'}},
@@ -69,6 +75,11 @@ export const DevSessionUpdate = {
                 name: {kind: 'Name', value: 'assetsUrl'},
                 value: {kind: 'Variable', name: {kind: 'Name', value: 'assetsUrl'}},
               },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'websocketUrl'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'websocketUrl'}},
+              },
               {
                 kind: 'Argument',
                 name: {kind: 'Name', value: 'manifest'},
diff --git a/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-create.graphql b/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-create.graphql
index d99cc3dddcc..f32b7fb9610 100644
--- a/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-create.graphql
+++ b/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-create.graphql
@@ -1,5 +1,5 @@
-mutation DevSessionCreate($appId: String!, $assetsUrl: String!) {
-  devSessionCreate(appId: $appId, assetsUrl: $assetsUrl) {
+mutation DevSessionCreate($appId: String!, $assetsUrl: String!, $websocketUrl: String) {
+  devSessionCreate(appId: $appId, assetsUrl: $assetsUrl, websocketUrl: $websocketUrl) {
     userErrors {
       message
       on
diff --git a/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-update.graphql b/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-update.graphql
index 6d58ddbf1c9..e0237c71c23 100644
--- a/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-update.graphql
+++ b/packages/app/src/cli/api/graphql/app-dev/queries/dev-session-update.graphql
@@ -1,5 +1,5 @@
-mutation DevSessionUpdate($appId: String!, $assetsUrl: String, $manifest: JSON, $inheritedModuleUids: [String!]!) {
-  devSessionUpdate(appId: $appId, assetsUrl: $assetsUrl, manifest: $manifest, inheritedModuleUids: $inheritedModuleUids) {
+mutation DevSessionUpdate($appId: String!, $assetsUrl: String, $websocketUrl: String, $manifest: JSON, $inheritedModuleUids: [String!]!) {
+  devSessionUpdate(appId: $appId, assetsUrl: $assetsUrl, websocketUrl: $websocketUrl, manifest: $manifest, inheritedModuleUids: $inheritedModuleUids) {
     userErrors {
       message
       on
diff --git a/packages/app/src/cli/api/graphql/business-platform-organizations/generated/types.d.ts b/packages/app/src/cli/api/graphql/business-platform-organizations/generated/types.d.ts
index af5f0d3a1b7..5a0339234cd 100644
--- a/packages/app/src/cli/api/graphql/business-platform-organizations/generated/types.d.ts
+++ b/packages/app/src/cli/api/graphql/business-platform-organizations/generated/types.d.ts
@@ -1,6 +1,4 @@
 /* eslint-disable @typescript-eslint/consistent-type-definitions, @typescript-eslint/naming-convention, @typescript-eslint/no-explicit-any  */
-import {JsonMapType} from '@shopify/cli-kit/node/toml'
-
 export type Maybe<T> = T | null
 export type InputMaybe<T> = Maybe<T>
 export type Exact<T extends {[key: string]: unknown}> = {[K in keyof T]: T[K]}
@@ -42,8 +40,6 @@ export type Scalars = {
   ISO8601Date: {input: any; output: any}
   /** An ISO 8601-encoded datetime */
   ISO8601DateTime: {input: any; output: any}
-  /** Represents untyped JSON */
-  JSON: {input: JsonMapType | string; output: JsonMapType}
   /** The ID for a LegalEntity. */
   LegalEntityID: {input: any; output: any}
   /** The ID for a OrganizationDomain. */
diff --git a/packages/app/src/cli/services/dev/extension.ts b/packages/app/src/cli/services/dev/extension.ts
index 59ec96db0d1..301f1313c4d 100644
--- a/packages/app/src/cli/services/dev/extension.ts
+++ b/packages/app/src/cli/services/dev/extension.ts
@@ -183,7 +183,7 @@ export async function devUIExtensions(options: ExtensionDevOptions): Promise<voi
   })
 }
 
-function getWebSocketUrl(url: ExtensionDevOptions['url']) {
+export function getWebSocketUrl(url: string) {
   const websocketURL = new URL('/extensions', url)
   websocketURL.protocol = 'wss:'
 
diff --git a/packages/app/src/cli/services/dev/extension/server/middlewares.ts b/packages/app/src/cli/services/dev/extension/server/middlewares.ts
index a2f179af568..7bf8116bc11 100644
--- a/packages/app/src/cli/services/dev/extension/server/middlewares.ts
+++ b/packages/app/src/cli/services/dev/extension/server/middlewares.ts
@@ -2,6 +2,7 @@ import {getExtensionPointRedirectUrl, getExtensionUrl, getRedirectUrl, sendError
 import {GetExtensionsMiddlewareOptions} from './models.js'
 import {getUIExtensionPayload} from '../payload.js'
 import {getHTML} from '../templates.js'
+import {getWebSocketUrl} from '../../extension.js'
 import {fileExists, isDirectory, readFile, findPathUp} from '@shopify/cli-kit/node/fs'
 import {IncomingMessage, ServerResponse, sendRedirect, send} from 'h3'
 import {joinPath, extname, moduleDirectory} from '@shopify/cli-kit/node/path'
@@ -199,7 +200,7 @@ export function getExtensionPayloadMiddleware({devOptions, getExtensions}: GetEx
           url: new URL('/extensions', devOptions.url).toString(),
         },
         socket: {
-          url: getWebsocketUrl(devOptions),
+          url: getWebSocketUrl(devOptions.url),
         },
         devConsole: {
           url: new URL('/extensions/dev-console', devOptions.url).toString(),
@@ -245,10 +246,3 @@ export function getExtensionPointMiddleware({devOptions, getExtensions}: GetExte
     await sendRedirect(response.event, url, 307)
   }
 }
-
-function getWebsocketUrl(devOptions: GetExtensionsMiddlewareOptions['devOptions']) {
-  const socket = new URL('/extensions', devOptions.url)
-  socket.protocol = 'wss:'
-
-  return socket.toString()
-}
diff --git a/packages/app/src/cli/services/dev/processes/dev-session/dev-session-process.test.ts b/packages/app/src/cli/services/dev/processes/dev-session/dev-session-process.test.ts
index 291f7951b0c..dff1edea298 100644
--- a/packages/app/src/cli/services/dev/processes/dev-session/dev-session-process.test.ts
+++ b/packages/app/src/cli/services/dev/processes/dev-session/dev-session-process.test.ts
@@ -90,9 +90,12 @@ describe('pushUpdatesForDevSession', () => {
     abortController = new AbortController()
     devSessionStatusManager = new DevSessionStatusManager()
     options = {
+      app: {} as AppLinkedInterface,
+      apiKey: 'test-api-key',
       developerPlatformClient,
       appWatcher,
       storeFqdn: 'test.myshopify.com',
+      url: 'https://test.dev',
       appId: 'app123',
       organizationId: 'org123',
       appPreviewURL: 'https://test.preview.url',
@@ -404,6 +407,7 @@ describe('pushUpdatesForDevSession', () => {
       appId: 'app123',
       // Assets URL is empty because the affected extension has no assets
       assetsUrl: undefined,
+      websocketUrl: 'wss://test.dev/extensions',
       manifest: {
         name: 'App',
         handle: '',
@@ -449,6 +453,7 @@ describe('pushUpdatesForDevSession', () => {
       shopFqdn: 'test.myshopify.com',
       appId: 'app123',
       assetsUrl: 'https://gcs.url',
+      websocketUrl: 'wss://test.dev/extensions',
       manifest: expect.any(Object),
       inheritedModuleUids: [],
     })
@@ -469,8 +474,7 @@ describe('pushUpdatesForDevSession', () => {
       shopFqdn: 'test.myshopify.com',
       appId: 'app123',
       assetsUrl: 'https://gcs.url',
-      manifest: expect.any(Object),
-      inheritedModuleUids: [],
+      websocketUrl: 'wss://test.dev/extensions',
     })
   })
 
diff --git a/packages/app/src/cli/services/dev/processes/dev-session/dev-session.ts b/packages/app/src/cli/services/dev/processes/dev-session/dev-session.ts
index 0572ed82db8..307e9a42dbf 100644
--- a/packages/app/src/cli/services/dev/processes/dev-session/dev-session.ts
+++ b/packages/app/src/cli/services/dev/processes/dev-session/dev-session.ts
@@ -5,6 +5,7 @@ import {AppEvent, AppEventWatcher, ExtensionEvent} from '../../app-events/app-ev
 import {compressBundle, getUploadURL, uploadToGCS, writeManifestToBundle} from '../../../bundle.js'
 import {DevSessionCreateOptions, DevSessionUpdateOptions} from '../../../../utilities/developer-platform-client.js'
 import {AppManifest} from '../../../../models/app/app.js'
+import {getWebSocketUrl} from '../../extension.js'
 import {endHRTimeInMs, startHRTime} from '@shopify/cli-kit/node/hrtime'
 import {ClientError} from 'graphql-request'
 import {JsonMapType} from '@shopify/cli-kit/node/toml'
@@ -276,16 +277,24 @@ export class DevSession {
       const {manifest, inheritedModuleUids, assets} = await this.createManifest(appEvent)
       const signedURL = await this.uploadAssetsIfNeeded(assets, !this.statusManager.status.isReady)
 
-      const payload = {
-        shopFqdn: this.options.storeFqdn,
-        appId: this.options.appId,
-        assetsUrl: signedURL,
-        manifest,
-        inheritedModuleUids,
-      }
+      const websocketUrl = getWebSocketUrl(this.options.url)
       if (this.statusManager.status.isReady) {
+        const payload: DevSessionUpdateOptions = {
+          shopFqdn: this.options.storeFqdn,
+          appId: this.options.appId,
+          assetsUrl: signedURL,
+          manifest,
+          inheritedModuleUids,
+          websocketUrl,
+        }
         return this.devSessionUpdateWithRetry(payload)
       } else {
+        const payload: DevSessionCreateOptions = {
+          shopFqdn: this.options.storeFqdn,
+          appId: this.options.appId,
+          assetsUrl: signedURL,
+          websocketUrl,
+        }
         return this.devSessionCreateWithRetry(payload)
       }
       // eslint-disable-next-line @typescript-eslint/no-explicit-any
diff --git a/packages/app/src/cli/utilities/developer-platform-client.ts b/packages/app/src/cli/utilities/developer-platform-client.ts
index a919f8e00e6..56f2f754f24 100644
--- a/packages/app/src/cli/utilities/developer-platform-client.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client.ts
@@ -163,13 +163,14 @@ interface DevSessionSharedOptions {
 
 export interface DevSessionCreateOptions extends DevSessionSharedOptions {
   assetsUrl?: string
-  manifest: AppManifest
+  websocketUrl?: string
 }
 
 export interface DevSessionUpdateOptions extends DevSessionSharedOptions {
   assetsUrl?: string
   manifest: AppManifest
   inheritedModuleUids: string[]
+  websocketUrl?: string
 }
 
 export type DevSessionDeleteOptions = DevSessionSharedOptions
diff --git a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
index f74ceebd240..b9990f35330 100644
--- a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
@@ -79,13 +79,19 @@ import {AppHomeSpecIdentifier} from '../../models/extensions/specifications/app_
 import {BrandingSpecIdentifier} from '../../models/extensions/specifications/app_config_branding.js'
 import {AppAccessSpecIdentifier} from '../../models/extensions/specifications/app_config_app_access.js'
 import {CONFIG_EXTENSION_IDS} from '../../models/extensions/extension-instance.js'
-import {DevSessionCreate, DevSessionCreateMutation} from '../../api/graphql/app-dev/generated/dev-session-create.js'
 import {
-  DevSessionUpdate,
+  DevSessionCreateDocument as DevSessionCreate,
+  DevSessionCreateMutation,
+} from '../../api/graphql/app-dev/generated/dev-session-create.js'
+import {
+  DevSessionUpdateDocument as DevSessionUpdate,
   DevSessionUpdateMutation,
   DevSessionUpdateMutationVariables,
 } from '../../api/graphql/app-dev/generated/dev-session-update.js'
-import {DevSessionDelete, DevSessionDeleteMutation} from '../../api/graphql/app-dev/generated/dev-session-delete.js'
+import {
+  DevSessionDeleteDocument as DevSessionDelete,
+  DevSessionDeleteMutation,
+} from '../../api/graphql/app-dev/generated/dev-session-delete.js'
 import {
   FetchDevStoreByDomain,
   FetchDevStoreByDomainQueryVariables,
@@ -1013,12 +1019,17 @@ export class AppManagementClient implements DeveloperPlatformClient {
     return appDeepLink({id, organizationId})
   }
 
-  async devSessionCreate({appId, assetsUrl, shopFqdn}: DevSessionCreateOptions): Promise<DevSessionCreateMutation> {
+  async devSessionCreate({
+    appId,
+    assetsUrl,
+    shopFqdn,
+    websocketUrl,
+  }: DevSessionCreateOptions): Promise<DevSessionCreateMutation> {
     const appIdNumber = String(numberFromGid(appId))
     return this.appDevRequest({
       query: DevSessionCreate,
       shopFqdn,
-      variables: {appId: appIdNumber, assetsUrl: assetsUrl ?? ''},
+      variables: {appId: appIdNumber, assetsUrl: assetsUrl ?? '', websocketUrl},
       requestOptions: {requestMode: 'slow-request'},
     })
   }
@@ -1029,6 +1040,7 @@ export class AppManagementClient implements DeveloperPlatformClient {
     shopFqdn,
     manifest,
     inheritedModuleUids,
+    websocketUrl,
   }: DevSessionUpdateOptions): Promise<DevSessionUpdateMutation> {
     const appIdNumber = String(numberFromGid(appId))
     const variables: DevSessionUpdateMutationVariables = {
@@ -1036,6 +1048,7 @@ export class AppManagementClient implements DeveloperPlatformClient {
       assetsUrl,
       manifest: JSON.stringify(manifest),
       inheritedModuleUids,
+      websocketUrl,
     }
     return this.appDevRequest({query: DevSessionUpdate, shopFqdn, variables})
   }