diff --git a/packages/app/src/cli/models/extensions/extension-instance.ts b/packages/app/src/cli/models/extensions/extension-instance.ts
index 6da9a76ebf7..1a495d3b022 100644
--- a/packages/app/src/cli/models/extensions/extension-instance.ts
+++ b/packages/app/src/cli/models/extensions/extension-instance.ts
@@ -285,7 +285,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
       return this.specification.devSessionWatchConfig(this)
     }
 
-    return this.specification.experience === 'configuration' ? {paths: []} : undefined
+    return this.isAppConfigExtension ? {paths: []} : undefined
   }
 
   async watchConfigurationPaths() {
diff --git a/packages/app/src/cli/models/extensions/specifications/admin.ts b/packages/app/src/cli/models/extensions/specifications/admin.ts
index e8b132e233b..f5002999372 100644
--- a/packages/app/src/cli/models/extensions/specifications/admin.ts
+++ b/packages/app/src/cli/models/extensions/specifications/admin.ts
@@ -7,11 +7,12 @@ const AdminSchema = zod.object({
   admin: zod
     .object({
       static_root: zod.string().optional(),
+      allowed_domains: zod.array(zod.string()).optional(),
     })
     .optional(),
 })
 
-type AdminConfigType = zod.infer<typeof AdminSchema> & BaseConfigType
+export type AdminConfigType = zod.infer<typeof AdminSchema> & BaseConfigType
 
 const adminSpecificationSpec = createExtensionSpecification<AdminConfigType>({
   identifier: 'admin',
@@ -33,6 +34,8 @@ const adminSpecificationSpec = createExtensionSpecification<AdminConfigType>({
       admin: {
         // eslint-disable-next-line @typescript-eslint/no-explicit-any
         static_root: (remoteContent as any).admin.static_root,
+        // eslint-disable-next-line @typescript-eslint/no-explicit-any
+        allowed_domains: (remoteContent as any).admin.allowed_domains,
       },
     }
   },
diff --git a/packages/app/src/cli/services/build/steps/include-assets-step.test.ts b/packages/app/src/cli/services/build/steps/include-assets-step.test.ts
index 6429801a725..ac4e89dfaba 100644
--- a/packages/app/src/cli/services/build/steps/include-assets-step.test.ts
+++ b/packages/app/src/cli/services/build/steps/include-assets-step.test.ts
@@ -1044,7 +1044,7 @@ describe('executeIncludeAssetsStep', () => {
       )
     })
 
-    test('throws when manifest.json already exists in the output directory', async () => {
+    test('overwrites manifest.json when it already exists in the output directory', async () => {
       // Given — a prior inclusion already copied a manifest.json to the output dir
       const contextWithConfig = {
         ...mockContext,
@@ -1056,8 +1056,7 @@ describe('executeIncludeAssetsStep', () => {
         } as unknown as ExtensionInstance,
       }
 
-      // Source files exist; output manifest.json already exists (simulating conflict);
-      // candidate output paths for tools.json are free so copyConfigKeyEntry succeeds.
+      // Source files exist; output manifest.json already exists
       vi.mocked(fs.fileExists).mockImplementation(async (path) => {
         const pathStr = String(path)
         return pathStr === '/test/output/manifest.json' || pathStr.startsWith('/test/extension/')
@@ -1081,10 +1080,9 @@ describe('executeIncludeAssetsStep', () => {
         },
       }
 
-      // When / Then — throws rather than silently overwriting
-      await expect(executeIncludeAssetsStep(step, contextWithConfig)).rejects.toThrow(
-        `Can't write manifest.json: a file already exists at '/test/output/manifest.json'`,
-      )
+      // When / Then — overwrites existing manifest.json
+      await expect(executeIncludeAssetsStep(step, contextWithConfig)).resolves.not.toThrow()
+      expect(fs.writeFile).toHaveBeenCalledWith('/test/output/manifest.json', expect.any(String))
     })
 
     test('writes an empty manifest when anchor resolves to a non-array value', async () => {
diff --git a/packages/app/src/cli/services/build/steps/include-assets/generate-manifest.ts b/packages/app/src/cli/services/build/steps/include-assets/generate-manifest.ts
index c39cc8b9529..20cdc405ead 100644
--- a/packages/app/src/cli/services/build/steps/include-assets/generate-manifest.ts
+++ b/packages/app/src/cli/services/build/steps/include-assets/generate-manifest.ts
@@ -1,6 +1,6 @@
 import {getNestedValue, tokenizePath} from './copy-config-key-entry.js'
 import {joinPath} from '@shopify/cli-kit/node/path'
-import {fileExists, mkdir, writeFile} from '@shopify/cli-kit/node/fs'
+import {mkdir, writeFile} from '@shopify/cli-kit/node/fs'
 import {outputDebug} from '@shopify/cli-kit/node/output'
 import type {BuildContext} from '../../client-steps.js'
 
@@ -20,7 +20,7 @@ interface ConfigKeyManifestEntry {
  * 3. Build root-level entries.
  * 4. Build grouped entries (anchor/groupBy logic) with path strings resolved
  *    via `resolveManifestPaths` using the copy-tracked `pathMap`.
- * 5. Write `outputDir/manifest.json`; throw if the file already exists.
+ * 5. Write `outputDir/manifest.json`, overwriting any existing file.
  *
  * @param pathMap - Map from raw config path values to their output-relative
  *   paths, as recorded during the copy phase by `copyConfigKeyEntry`.
@@ -113,12 +113,6 @@ export async function generateManifestFile(
   }
 
   const manifestPath = joinPath(outputDir, 'manifest.json')
-  if (await fileExists(manifestPath)) {
-    throw new Error(
-      `Can't write manifest.json: a file already exists at '${manifestPath}'. ` +
-        `Remove or rename the conflicting inclusion to avoid overwriting the generated manifest.`,
-    )
-  }
   await mkdir(outputDir)
   await writeFile(manifestPath, JSON.stringify(manifest, null, 2))
   outputDebug(`Generated manifest.json in ${outputDir}\n`, options.stdout)
diff --git a/packages/app/src/cli/services/dev/app-events/file-watcher.ts b/packages/app/src/cli/services/dev/app-events/file-watcher.ts
index ca55158bae2..6b022e82cf2 100644
--- a/packages/app/src/cli/services/dev/app-events/file-watcher.ts
+++ b/packages/app/src/cli/services/dev/app-events/file-watcher.ts
@@ -150,7 +150,7 @@ export class FileWatcher {
   private getAllWatchedFiles(): string[] {
     this.extensionWatchedFiles.clear()
 
-    const extensionResults = this.app.nonConfigExtensions.map((extension) => ({
+    const extensionResults = this.app.realExtensions.map((extension) => ({
       extension,
       watchedFiles: extension.watchedFiles(),
     }))
diff --git a/packages/app/src/cli/services/dev/extension.test.ts b/packages/app/src/cli/services/dev/extension.test.ts
index a6b696159bf..f63ce543464 100644
--- a/packages/app/src/cli/services/dev/extension.test.ts
+++ b/packages/app/src/cli/services/dev/extension.test.ts
@@ -33,7 +33,14 @@ describe('devUIExtensions()', () => {
 
     // eslint-disable-next-line @typescript-eslint/ban-ts-comment
     // @ts-ignore
-    vi.spyOn(store, 'ExtensionsPayloadStore').mockImplementation(() => ({mock: 'payload-store'}))
+    vi.spyOn(store, 'ExtensionsPayloadStore').mockImplementation(
+      () =>
+        ({
+          mock: 'payload-store',
+          updateAdminConfigFromExtensionEvents: vi.fn(),
+          getAppAssets: vi.fn(),
+        }) as unknown as store.ExtensionsPayloadStore,
+    )
     vi.spyOn(server, 'setupHTTPServer').mockReturnValue({
       mock: 'http-server',
       close: serverCloseSpy,
@@ -67,8 +74,9 @@ describe('devUIExtensions()', () => {
     // THEN
     expect(server.setupHTTPServer).toHaveBeenCalledWith({
       devOptions: {...options, websocketURL: 'wss://mock.url/extensions'},
-      payloadStore: {mock: 'payload-store'},
+      payloadStore: expect.objectContaining({mock: 'payload-store'}),
       getExtensions: expect.any(Function),
+      getAppAssets: expect.any(Function),
     })
   })
 
@@ -94,7 +102,7 @@ describe('devUIExtensions()', () => {
     expect(websocket.setupWebsocketConnection).toHaveBeenCalledWith({
       ...options,
       httpServer: expect.objectContaining({mock: 'http-server'}),
-      payloadStore: {mock: 'payload-store'},
+      payloadStore: expect.objectContaining({mock: 'payload-store'}),
       websocketURL: 'wss://mock.url/extensions',
     })
   })
diff --git a/packages/app/src/cli/services/dev/extension.ts b/packages/app/src/cli/services/dev/extension.ts
index 301f1313c4d..49aae24d55c 100644
--- a/packages/app/src/cli/services/dev/extension.ts
+++ b/packages/app/src/cli/services/dev/extension.ts
@@ -35,7 +35,8 @@ export interface ExtensionDevOptions {
   buildDirectory?: string
 
   /**
-   * The extension to be built.
+   * All real extensions in the app, including non-previewable ones (e.g., admin config).
+   * Previewable extensions are filtered internally for the UI payload.
    */
   extensions: ExtensionInstance[]
 
@@ -126,14 +127,20 @@ export async function devUIExtensions(options: ExtensionDevOptions): Promise<voi
   const bundlePath = payloadOptions.appWatcher.buildOutputPath
   const payloadStoreRawPayload = await getExtensionsPayloadStoreRawPayload(payloadOptions, bundlePath)
   const payloadStore = new ExtensionsPayloadStore(payloadStoreRawPayload, payloadOptions)
-  let extensions = payloadOptions.extensions
+  let extensions = payloadOptions.extensions.filter((ext) => ext.isPreviewable)
 
   const getExtensions = () => {
     return extensions
   }
 
   outputDebug(`Setting up the UI extensions HTTP server...`, payloadOptions.stdout)
-  const httpServer = setupHTTPServer({devOptions: payloadOptions, payloadStore, getExtensions})
+  const getAppAssets = () => payloadStore.getAppAssets()
+  const httpServer = setupHTTPServer({
+    devOptions: payloadOptions,
+    payloadStore,
+    getExtensions,
+    getAppAssets,
+  })
 
   outputDebug(`Setting up the UI extensions Websocket server...`, payloadOptions.stdout)
   const websocketConnection = setupWebsocketConnection({...payloadOptions, httpServer, payloadStore})
@@ -144,6 +151,8 @@ export async function devUIExtensions(options: ExtensionDevOptions): Promise<voi
       extensions = app.allExtensions.filter((ext) => ext.isPreviewable)
     }
 
+    payloadStore.updateAdminConfigFromExtensionEvents(extensionEvents)
+
     for (const event of extensionEvents) {
       if (!event.extension.isPreviewable) continue
       const status = event.buildResult?.status === 'ok' ? 'success' : 'error'
diff --git a/packages/app/src/cli/services/dev/extension/payload/models.ts b/packages/app/src/cli/services/dev/extension/payload/models.ts
index 796f93108bd..487f29e58c6 100644
--- a/packages/app/src/cli/services/dev/extension/payload/models.ts
+++ b/packages/app/src/cli/services/dev/extension/payload/models.ts
@@ -8,6 +8,13 @@ interface ExtensionsPayloadInterface {
     url: string
     mobileUrl: string
     title: string
+    allowed_domains?: string[]
+    assets?: {
+      [key: string]: {
+        url: string
+        lastUpdated: number
+      }
+    }
   }
   appId?: string
   store: string
diff --git a/packages/app/src/cli/services/dev/extension/payload/store.test.ts b/packages/app/src/cli/services/dev/extension/payload/store.test.ts
index cd9a5229da8..f48e70a04d5 100644
--- a/packages/app/src/cli/services/dev/extension/payload/store.test.ts
+++ b/packages/app/src/cli/services/dev/extension/payload/store.test.ts
@@ -7,8 +7,18 @@ import {
 import {UIExtensionPayload, ExtensionsEndpointPayload} from './models.js'
 import * as payload from '../payload.js'
 import {ExtensionInstance} from '../../../../models/extensions/extension-instance.js'
+import {ExtensionEvent} from '../../app-events/app-event-watcher.js'
 import {beforeEach, describe, expect, test, vi} from 'vitest'
 
+function createAdminExtension(config: {static_root?: string; allowed_domains?: string[]} = {}) {
+  return {
+    type: 'admin',
+    isPreviewable: false,
+    configuration: {admin: config},
+    specification: {},
+  } as unknown as ExtensionInstance
+}
+
 describe('getExtensionsPayloadStoreRawPayload()', () => {
   test('returns the raw payload', async () => {
     // Given
@@ -21,7 +31,11 @@ describe('getExtensionsPayloadStoreRawPayload()', () => {
       appName: 'mock-app-name',
       url: 'https://mock-url.com',
       websocketURL: 'wss://mock-websocket-url.com',
-      extensions: [{}, {}, {}],
+      extensions: [
+        {specification: {}, isPreviewable: true},
+        {specification: {}, isPreviewable: true},
+        {specification: {}, isPreviewable: true},
+      ],
       storeFqdn: 'mock-store-fqdn.myshopify.com',
       manifestVersion: '3',
     } as unknown as ExtensionsPayloadStoreOptions
@@ -52,10 +66,86 @@ describe('getExtensionsPayloadStoreRawPayload()', () => {
       extensions: [{mock: 'extension-payload'}, {mock: 'extension-payload'}, {mock: 'extension-payload'}],
     })
   })
+
+  test('includes allowed_domains and assets when admin extension is present', async () => {
+    // Given
+    vi.spyOn(payload, 'getUIExtensionPayload').mockResolvedValue({mock: 'ext'} as unknown as UIExtensionPayload)
+    const adminExt = createAdminExtension({static_root: 'public', allowed_domains: ['https://cdn.example.com']})
+    const previewableExt = {specification: {}, isPreviewable: true} as unknown as ExtensionInstance
+
+    const options = {
+      apiKey: 'api-key',
+      appName: 'my-app',
+      url: 'https://tunnel.example.com',
+      websocketURL: 'wss://tunnel.example.com',
+      extensions: [previewableExt, adminExt],
+      storeFqdn: 'store.myshopify.com',
+      manifestVersion: '3',
+    } as unknown as ExtensionsPayloadStoreOptions
+
+    // When
+    const rawPayload = await getExtensionsPayloadStoreRawPayload(options, 'bundle-path')
+
+    // Then
+    expect(rawPayload.app.allowed_domains).toStrictEqual(['https://cdn.example.com'])
+    expect(rawPayload.app.assets).toStrictEqual({
+      staticRoot: {
+        url: 'https://tunnel.example.com/extensions/assets/staticRoot/',
+        lastUpdated: expect.any(Number),
+      },
+    })
+    // Admin extension should not appear in the UI extensions payload
+    expect(rawPayload.extensions).toHaveLength(1)
+  })
+
+  test('does not include assets or allowed_domains when no admin extension exists', async () => {
+    // Given
+    vi.spyOn(payload, 'getUIExtensionPayload').mockResolvedValue({mock: 'ext'} as unknown as UIExtensionPayload)
+
+    const options = {
+      apiKey: 'api-key',
+      appName: 'my-app',
+      url: 'https://tunnel.example.com',
+      websocketURL: 'wss://tunnel.example.com',
+      extensions: [{specification: {}, isPreviewable: true}],
+      storeFqdn: 'store.myshopify.com',
+      manifestVersion: '3',
+    } as unknown as ExtensionsPayloadStoreOptions
+
+    // When
+    const rawPayload = await getExtensionsPayloadStoreRawPayload(options, 'bundle-path')
+
+    // Then
+    expect(rawPayload.app.allowed_domains).toBeUndefined()
+    expect(rawPayload.app.assets).toBeUndefined()
+  })
+
+  test('includes allowed_domains but not assets when admin has no static_root', async () => {
+    // Given
+    vi.spyOn(payload, 'getUIExtensionPayload').mockResolvedValue({mock: 'ext'} as unknown as UIExtensionPayload)
+    const adminExt = createAdminExtension({allowed_domains: ['https://cdn.example.com']})
+
+    const options = {
+      apiKey: 'api-key',
+      appName: 'my-app',
+      url: 'https://tunnel.example.com',
+      websocketURL: 'wss://tunnel.example.com',
+      extensions: [adminExt],
+      storeFqdn: 'store.myshopify.com',
+      manifestVersion: '3',
+    } as unknown as ExtensionsPayloadStoreOptions
+
+    // When
+    const rawPayload = await getExtensionsPayloadStoreRawPayload(options, 'bundle-path')
+
+    // Then
+    expect(rawPayload.app.allowed_domains).toStrictEqual(['https://cdn.example.com'])
+    expect(rawPayload.app.assets).toBeUndefined()
+  })
 })
 
 describe('ExtensionsPayloadStore()', () => {
-  const mockOptions = {} as unknown as ExtensionsPayloadStoreOptions
+  const mockOptions = {extensions: []} as unknown as ExtensionsPayloadStoreOptions
 
   test('getRawPayload() returns the raw payload', async () => {
     // Given
@@ -365,4 +455,95 @@ describe('ExtensionsPayloadStore()', () => {
       expect(onUpdateSpy).not.toHaveBeenCalled()
     })
   })
+
+  describe('getAppAssets()', () => {
+    test('returns asset directories when admin extension has static_root', () => {
+      const adminExt = createAdminExtension({static_root: 'public'})
+      const options = {extensions: [adminExt], appDirectory: '/app'} as unknown as ExtensionsPayloadStoreOptions
+      const store = new ExtensionsPayloadStore({extensions: []} as unknown as ExtensionsEndpointPayload, options)
+
+      expect(store.getAppAssets()).toStrictEqual({staticRoot: '/app/public'})
+    })
+
+    test('returns undefined when no admin extension exists', () => {
+      const store = new ExtensionsPayloadStore({extensions: []} as unknown as ExtensionsEndpointPayload, mockOptions)
+
+      expect(store.getAppAssets()).toBeUndefined()
+    })
+
+    test('returns undefined when admin extension has no static_root', () => {
+      const adminExt = createAdminExtension({allowed_domains: ['https://example.com']})
+      const options = {extensions: [adminExt], appDirectory: '/app'} as unknown as ExtensionsPayloadStoreOptions
+      const store = new ExtensionsPayloadStore({extensions: []} as unknown as ExtensionsEndpointPayload, options)
+
+      expect(store.getAppAssets()).toBeUndefined()
+    })
+  })
+
+  describe('updateAdminConfigFromExtensionEvents()', () => {
+    test('updates allowed_domains and bumps asset timestamps on admin change', () => {
+      // Given
+      const adminExt = createAdminExtension({allowed_domains: ['https://new.example.com'], static_root: 'public'})
+      const options = {extensions: [adminExt], appDirectory: '/app'} as unknown as ExtensionsPayloadStoreOptions
+      const initialPayload = {
+        app: {
+          allowed_domains: ['https://old.example.com'],
+          assets: {staticRoot: {url: 'https://tunnel/extensions/assets/staticRoot/', lastUpdated: 1000}},
+        },
+        extensions: [],
+      } as unknown as ExtensionsEndpointPayload
+
+      const store = new ExtensionsPayloadStore(initialPayload, options)
+      const onUpdateSpy = vi.fn()
+      store.on(ExtensionsPayloadStoreEvent.Update, onUpdateSpy)
+
+      // When
+      store.updateAdminConfigFromExtensionEvents([{extension: adminExt} as unknown as ExtensionEvent])
+
+      // Then
+      const result = store.getRawPayload()
+      expect(result.app.allowed_domains).toStrictEqual(['https://new.example.com'])
+      expect(result.app.assets!.staticRoot!.lastUpdated).toBeGreaterThan(1000)
+      expect(onUpdateSpy).toHaveBeenCalledWith([])
+    })
+
+    test('clears allowed_domains when admin config removes them', () => {
+      // Given
+      const adminExt = createAdminExtension({static_root: 'public'})
+      const options = {extensions: [adminExt], appDirectory: '/app'} as unknown as ExtensionsPayloadStoreOptions
+      const initialPayload = {
+        app: {allowed_domains: ['https://old.example.com'], assets: {}},
+        extensions: [],
+      } as unknown as ExtensionsEndpointPayload
+
+      const store = new ExtensionsPayloadStore(initialPayload, options)
+
+      // When
+      store.updateAdminConfigFromExtensionEvents([{extension: adminExt} as unknown as ExtensionEvent])
+
+      // Then
+      expect(store.getRawPayload().app.allowed_domains).toBeUndefined()
+    })
+
+    test('does nothing when no admin extension event is present', () => {
+      // Given
+      const store = new ExtensionsPayloadStore(
+        {app: {allowed_domains: ['https://example.com']}, extensions: []} as unknown as ExtensionsEndpointPayload,
+        mockOptions,
+      )
+      const onUpdateSpy = vi.fn()
+      store.on(ExtensionsPayloadStoreEvent.Update, onUpdateSpy)
+
+      const nonAdminEvent = {
+        extension: {type: 'ui_extension'},
+      } as unknown as ExtensionEvent
+
+      // When
+      store.updateAdminConfigFromExtensionEvents([nonAdminEvent])
+
+      // Then
+      expect(store.getRawPayload().app.allowed_domains).toStrictEqual(['https://example.com'])
+      expect(onUpdateSpy).not.toHaveBeenCalled()
+    })
+  })
 })
diff --git a/packages/app/src/cli/services/dev/extension/payload/store.ts b/packages/app/src/cli/services/dev/extension/payload/store.ts
index ae4919485c1..1b9345f5d2a 100644
--- a/packages/app/src/cli/services/dev/extension/payload/store.ts
+++ b/packages/app/src/cli/services/dev/extension/payload/store.ts
@@ -3,6 +3,9 @@ import {ExtensionDevOptions} from '../../extension.js'
 import {getUIExtensionPayload, isNewExtensionPointsSchema} from '../payload.js'
 import {buildAppURLForMobile, buildAppURLForWeb} from '../../../../utilities/app/app-url.js'
 import {ExtensionInstance} from '../../../../models/extensions/extension-instance.js'
+import {AdminConfigType} from '../../../../models/extensions/specifications/admin.js'
+import {ExtensionEvent} from '../../app-events/app-event-watcher.js'
+import {joinPath} from '@shopify/cli-kit/node/path'
 import {deepMergeObjects} from '@shopify/cli-kit/common/object'
 import {outputDebug, outputContent} from '@shopify/cli-kit/node/output'
 import {EventEmitter} from 'events'
@@ -11,6 +14,21 @@ export interface ExtensionsPayloadStoreOptions extends ExtensionDevOptions {
   websocketURL: string
 }
 
+interface AdminConfig {
+  allowedDomains?: string[]
+  staticRoot?: string
+}
+
+function getAdminConfig(extensions: ExtensionInstance[]): AdminConfig | undefined {
+  const adminExtension = extensions.find((ext) => ext.type === 'admin')
+  if (!adminExtension) return undefined
+  const admin = (adminExtension.configuration as AdminConfigType).admin
+  return {
+    allowedDomains: admin?.allowed_domains,
+    staticRoot: admin?.static_root,
+  }
+}
+
 export enum ExtensionsPayloadStoreEvent {
   Update = 'PayloadUpdatedEvent:UPDATE',
 }
@@ -19,7 +37,7 @@ export async function getExtensionsPayloadStoreRawPayload(
   options: Omit<ExtensionsPayloadStoreOptions, 'appWatcher'>,
   bundlePath: string,
 ): Promise<ExtensionsEndpointPayload> {
-  return {
+  const payload: ExtensionsEndpointPayload = {
     app: {
       title: options.appName,
       apiKey: options.apiKey,
@@ -38,18 +56,46 @@ export async function getExtensionsPayloadStoreRawPayload(
       url: new URL('/extensions/dev-console', options.url).toString(),
     },
     store: options.storeFqdn,
-    extensions: await Promise.all(options.extensions.map((ext) => getUIExtensionPayload(ext, bundlePath, options))),
+    extensions: await Promise.all(
+      options.extensions
+        .filter((ext) => ext.isPreviewable)
+        .map((ext) => getUIExtensionPayload(ext, bundlePath, options)),
+    ),
   }
+
+  // Admin extension contributes app-level config to the payload
+  const adminConfig = getAdminConfig(options.extensions)
+  if (adminConfig) {
+    payload.app.allowed_domains = adminConfig.allowedDomains
+    if (adminConfig.staticRoot) {
+      const assetKey = 'staticRoot'
+      payload.app.assets = {
+        [assetKey]: {
+          url: new URL(`/extensions/assets/${assetKey}/`, options.url).toString(),
+          lastUpdated: Date.now(),
+        },
+      }
+    }
+  }
+
+  return payload
 }
 
 export class ExtensionsPayloadStore extends EventEmitter {
   private readonly options: ExtensionsPayloadStoreOptions
   private rawPayload: ExtensionsEndpointPayload
+  private appAssetDirectories: Record<string, string> | undefined
 
   constructor(rawPayload: ExtensionsEndpointPayload, options: ExtensionsPayloadStoreOptions) {
     super()
     this.rawPayload = rawPayload
     this.options = options
+
+    this.refreshAppAssetDirectories()
+  }
+
+  getAppAssets(): Record<string, string> | undefined {
+    return this.appAssetDirectories
   }
 
   getConnectedPayload() {
@@ -170,6 +216,30 @@ export class ExtensionsPayloadStore extends EventEmitter {
     this.emitUpdate([extension.devUUID])
   }
 
+  updateAdminConfigFromExtensionEvents(extensionEvents: ExtensionEvent[]) {
+    const adminEvent = extensionEvents.find((event) => event.extension.type === 'admin')
+    if (!adminEvent) return
+
+    const adminConfig = getAdminConfig([adminEvent.extension])
+    this.rawPayload.app.allowed_domains = adminConfig?.allowedDomains
+
+    this.refreshAppAssetDirectories()
+    if (this.rawPayload.app.assets) {
+      for (const key of Object.keys(this.rawPayload.app.assets)) {
+        this.rawPayload.app.assets[key]!.lastUpdated = Date.now()
+      }
+    }
+
+    this.emitUpdate([])
+  }
+
+  private refreshAppAssetDirectories() {
+    const adminConfig = getAdminConfig(this.options.extensions)
+    this.appAssetDirectories = adminConfig?.staticRoot
+      ? {staticRoot: joinPath(this.options.appDirectory, adminConfig.staticRoot)}
+      : undefined
+  }
+
   private emitUpdate(extensionIds: string[]) {
     this.emit(ExtensionsPayloadStoreEvent.Update, extensionIds)
   }
diff --git a/packages/app/src/cli/services/dev/extension/server.ts b/packages/app/src/cli/services/dev/extension/server.ts
index 456c8364c61..b7a5bd7adec 100644
--- a/packages/app/src/cli/services/dev/extension/server.ts
+++ b/packages/app/src/cli/services/dev/extension/server.ts
@@ -2,6 +2,7 @@ import {
   corsMiddleware,
   devConsoleAssetsMiddleware,
   devConsoleIndexMiddleware,
+  getAppAssetsMiddleware,
   getExtensionAssetMiddleware,
   getExtensionPayloadMiddleware,
   getExtensionPointMiddleware,
@@ -19,6 +20,7 @@ interface SetupHTTPServerOptions {
   devOptions: ExtensionsPayloadStoreOptions
   payloadStore: ExtensionsPayloadStore
   getExtensions: () => ExtensionInstance[]
+  getAppAssets?: () => Record<string, string> | undefined
 }
 
 export function setupHTTPServer(options: SetupHTTPServerOptions) {
@@ -28,6 +30,9 @@ export function setupHTTPServer(options: SetupHTTPServerOptions) {
   httpApp.use(getLogMiddleware(options))
   httpApp.use(corsMiddleware)
   httpApp.use(noCacheMiddleware)
+  if (options.getAppAssets) {
+    httpRouter.use('/extensions/assets/:assetKey/**:filePath', getAppAssetsMiddleware(options.getAppAssets))
+  }
   httpRouter.use('/extensions/dev-console', devConsoleIndexMiddleware)
   httpRouter.use('/extensions/dev-console/assets/**:assetPath', devConsoleAssetsMiddleware)
   httpRouter.use('/extensions/:extensionId', getExtensionPayloadMiddleware(options))
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 ed17a0f474d..c7ab7e8967f 100644
--- a/packages/app/src/cli/services/dev/extension/server/middlewares.ts
+++ b/packages/app/src/cli/services/dev/extension/server/middlewares.ts
@@ -5,7 +5,7 @@ import {getHTML} from '../templates.js'
 import {getWebSocketUrl} from '../../extension.js'
 import {fileExists, isDirectory, readFile, findPathUp} from '@shopify/cli-kit/node/fs'
 import {sendRedirect, defineEventHandler, getRequestHeader, getRouterParams, setResponseHeader} from 'h3'
-import {joinPath, dirname, extname, moduleDirectory} from '@shopify/cli-kit/node/path'
+import {joinPath, resolvePath, dirname, extname, moduleDirectory} from '@shopify/cli-kit/node/path'
 import {outputDebug} from '@shopify/cli-kit/node/output'
 
 import type {H3Event} from 'h3'
@@ -134,6 +134,25 @@ export const devConsoleAssetsMiddleware = defineEventHandler(async (event) => {
   })
 })
 
+export function getAppAssetsMiddleware(getAppAssets: () => Record<string, string> | undefined) {
+  return defineEventHandler(async (event) => {
+    const {assetKey = '', filePath = ''} = getRouterParams(event)
+    const appAssets = getAppAssets()
+    const directory = appAssets?.[assetKey]
+    if (!directory) {
+      return sendError(event, {statusCode: 404, statusMessage: `No app assets configured for key: ${assetKey}`})
+    }
+    const resolvedDirectory = resolvePath(directory)
+    const resolvedFilePath = resolvePath(directory, filePath)
+    if (!resolvedFilePath.startsWith(resolvedDirectory)) {
+      return sendError(event, {statusCode: 403, statusMessage: 'Path traversal is not allowed'})
+    }
+    return fileServerMiddleware(event, {
+      filePath: resolvedFilePath,
+    })
+  })
+}
+
 export function getLogMiddleware({devOptions}: GetExtensionsMiddlewareOptions) {
   return defineEventHandler((event) => {
     outputDebug(`UI extensions server received a ${event.method} request to URL ${event.path}`, devOptions.stdout)
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 1e9602ce520..cb7cf9d8a0c 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
@@ -351,6 +351,12 @@ export class DevSession {
       .filter((event) => event.type !== 'deleted')
       .map((event) => event.extension.uid)
 
+    // WORKAROUND. This is a temporary fix because `admin` is not compatible with inheritedUids in Core.
+    // It needs to be included in the manifest always if present in the app.
+    if (appEvent.app.allExtensions.some((ext) => ext.type === 'admin') && !updatedUids.includes('admin')) {
+      updatedUids.push('admin')
+    }
+
     const nonUpdatedUids = appEvent.app.allExtensions
       .filter((ext) => !updatedUids.includes(ext.uid))
       .map((ext) => ext.uid)
diff --git a/packages/app/src/cli/services/dev/processes/previewable-extension.ts b/packages/app/src/cli/services/dev/processes/previewable-extension.ts
index 387d97ebeed..c6e064ba1d4 100644
--- a/packages/app/src/cli/services/dev/processes/previewable-extension.ts
+++ b/packages/app/src/cli/services/dev/processes/previewable-extension.ts
@@ -22,7 +22,7 @@ interface PreviewableExtensionOptions {
   appDirectory: string
   appId?: string
   grantedScopes: string[]
-  previewableExtensions: ExtensionInstance[]
+  allExtensions: ExtensionInstance[]
   appWatcher: AppEventWatcher
 }
 
@@ -44,7 +44,7 @@ export const launchPreviewableExtensionProcess: DevProcessFunction<PreviewableEx
     appDotEnvFile,
     appId,
     grantedScopes,
-    previewableExtensions,
+    allExtensions,
     appDirectory,
     appWatcher,
   },
@@ -54,7 +54,7 @@ export const launchPreviewableExtensionProcess: DevProcessFunction<PreviewableEx
     appDotEnvFile,
     appDirectory,
     id: appId,
-    extensions: previewableExtensions,
+    extensions: allExtensions,
     stdout,
     stderr,
     signal: abortSignal,
@@ -76,7 +76,7 @@ export async function setupPreviewableExtensionsProcess({
   storeFqdn,
   checkoutCartUrl,
   ...options
-}: Omit<PreviewableExtensionOptions, 'pathPrefix' | 'previewableExtensions' | 'port' | 'cartUrl'> & {
+}: Omit<PreviewableExtensionOptions, 'pathPrefix' | 'allExtensions' | 'port' | 'cartUrl'> & {
   allExtensions: ExtensionInstance[]
   checkoutCartUrl?: string
 }): Promise<PreviewableExtensionProcess | undefined> {
@@ -92,7 +92,7 @@ export async function setupPreviewableExtensionsProcess({
       pathPrefix: '/extensions',
       port: -1,
       storeFqdn,
-      previewableExtensions,
+      allExtensions,
       cartUrl,
       ...options,
     },
diff --git a/packages/app/src/cli/services/dev/processes/setup-dev-processes.test.ts b/packages/app/src/cli/services/dev/processes/setup-dev-processes.test.ts
index add3d387079..aeb6702a4ea 100644
--- a/packages/app/src/cli/services/dev/processes/setup-dev-processes.test.ts
+++ b/packages/app/src/cli/services/dev/processes/setup-dev-processes.test.ts
@@ -220,7 +220,7 @@ describe('setup-dev-processes', () => {
       prefix: 'extensions',
       options: {
         apiKey: 'api-key',
-        previewableExtensions: [previewable],
+        allExtensions: expect.arrayContaining([previewable]),
         storeFqdn,
         proxyUrl: 'https://example.com/proxy',
         port: expect.any(Number),
diff --git a/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts b/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
index 9a2a3723740..a7ece06e3dc 100644
--- a/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
+++ b/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
@@ -149,7 +149,7 @@ export async function setupDevProcesses({
         })
       : undefined,
     await setupPreviewableExtensionsProcess({
-      allExtensions: reloadedApp.allExtensions,
+      allExtensions: reloadedApp.realExtensions,
       storeFqdn,
       storeId,
       apiKey,
diff --git a/packages/ui-extensions-server-kit/src/types.ts b/packages/ui-extensions-server-kit/src/types.ts
index e2ef8e8eb61..46a09de168f 100644
--- a/packages/ui-extensions-server-kit/src/types.ts
+++ b/packages/ui-extensions-server-kit/src/types.ts
@@ -182,4 +182,11 @@ export interface App {
   }
   supportEmail?: string
   supportLocales?: string[]
+  allowed_domains?: string[]
+  assets?: {
+    [key: string]: {
+      url: string
+      lastUpdated: number
+    }
+  }
 }