diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.test.ts b/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.test.ts
index c45f98bdf6..665b3d9a9e 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.test.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.test.ts
@@ -7,9 +7,9 @@ vi.mock('@shopify/cli-kit/node/fs')
 
 describe('hosted_app_home', () => {
   describe('transform', () => {
-    test('should return the transformed object with static_root', () => {
+    test('should return the transformed object with static_root (local admin subsection to flat remote)', () => {
       const object = {
-        static_root: 'public',
+        admin: {static_root: 'public'},
       }
       const appConfigSpec = spec
 
@@ -20,7 +20,7 @@ describe('hosted_app_home', () => {
       })
     })
 
-    test('should return empty object when static_root is not provided', () => {
+    test('should return empty object when admin.static_root is not provided', () => {
       const object = {}
       const appConfigSpec = spec
 
@@ -31,7 +31,7 @@ describe('hosted_app_home', () => {
   })
 
   describe('reverseTransform', () => {
-    test('should return the reversed transformed object with static_root', () => {
+    test('should return the reversed transformed object (flat remote to local admin subsection)', () => {
       const object = {
         static_root: 'public',
       }
@@ -40,7 +40,7 @@ describe('hosted_app_home', () => {
       const result = appConfigSpec.transformRemoteToLocal!(object)
 
       expect(result).toMatchObject({
-        static_root: 'public',
+        admin: {static_root: 'public'},
       })
     })
 
@@ -57,7 +57,7 @@ describe('hosted_app_home', () => {
   describe('copyStaticAssets', () => {
     test('should copy static assets from source to output directory', async () => {
       vi.mocked(copyDirectoryContents).mockResolvedValue(undefined)
-      const config = {static_root: 'public'}
+      const config = {admin: {static_root: 'public'}}
       const directory = '/app/root'
       const outputPath = '/output/dist/bundle.js'
 
@@ -66,7 +66,7 @@ describe('hosted_app_home', () => {
       expect(copyDirectoryContents).toHaveBeenCalledWith('/app/root/public', '/output/dist')
     })
 
-    test('should not copy assets when static_root is not provided', async () => {
+    test('should not copy assets when admin.static_root is not provided', async () => {
       const config = {}
       const directory = '/app/root'
       const outputPath = '/output/dist/bundle.js'
@@ -78,7 +78,7 @@ describe('hosted_app_home', () => {
 
     test('should throw error when copy fails', async () => {
       vi.mocked(copyDirectoryContents).mockRejectedValue(new Error('Permission denied'))
-      const config = {static_root: 'public'}
+      const config = {admin: {static_root: 'public'}}
       const directory = '/app/root'
       const outputPath = '/output/dist/bundle.js'
 
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.ts b/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.ts
index 6b71b71049..9b608fcef6 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_hosted_app_home.ts
@@ -5,11 +5,15 @@ import {dirname, joinPath} from '@shopify/cli-kit/node/path'
 import {zod} from '@shopify/cli-kit/node/schema'
 
 const HostedAppHomeSchema = BaseSchemaWithoutHandle.extend({
-  static_root: zod.string().optional(),
+  admin: zod
+    .object({
+      static_root: zod.string().optional(),
+    })
+    .optional(),
 })
 
 const HostedAppHomeTransformConfig: TransformationConfig = {
-  static_root: 'static_root',
+  static_root: 'admin.static_root',
 }
 
 export const HostedAppHomeSpecIdentifier = 'hosted_app_home'
@@ -20,8 +24,9 @@ const hostedAppHomeSpec = createConfigExtensionSpecification({
   schema: HostedAppHomeSchema,
   transformConfig: HostedAppHomeTransformConfig,
   copyStaticAssets: async (config, directory, outputPath) => {
-    if (!config.static_root) return
-    const sourceDir = joinPath(directory, config.static_root)
+    const staticRoot = config.admin?.static_root
+    if (!staticRoot) return
+    const sourceDir = joinPath(directory, staticRoot)
     const outputDir = dirname(outputPath)
 
     return copyDirectoryContents(sourceDir, outputDir).catch((error) => {