diff --git a/packages/app/src/cli/models/extensions/extension-instance.test.ts b/packages/app/src/cli/models/extensions/extension-instance.test.ts
index 5a808958df9..dbafca2026a 100644
--- a/packages/app/src/cli/models/extensions/extension-instance.test.ts
+++ b/packages/app/src/cli/models/extensions/extension-instance.test.ts
@@ -72,10 +72,10 @@ describe('keepBuiltSourcemapsLocally', async () => {
 
         await extensionInstance.keepBuiltSourcemapsLocally(bundleDirectory)
 
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js.map'))).toBe(true)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js.map'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'uid1', 'scriptToMove.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'uid1', 'scriptToMove.js.map'))).toBe(true)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js.map'))).toBe(false)
       })
     })
   })
@@ -103,10 +103,10 @@ describe('keepBuiltSourcemapsLocally', async () => {
 
         await extensionInstance.keepBuiltSourcemapsLocally(bundleInputPath)
 
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js.map'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js.map'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'wrongUID', 'scriptToMove.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'wrongUID', 'scriptToMove.js.map'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js.map'))).toBe(false)
       })
     })
   })
@@ -133,10 +133,10 @@ describe('keepBuiltSourcemapsLocally', async () => {
 
         await extensionInstance.keepBuiltSourcemapsLocally(bundleDirectory)
 
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToMove.js.map'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js'))).toBe(false)
-        expect(fileExistsSync(joinPath(outputPath, 'dist', 'scriptToIgnore.js.map'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'uid1', 'scriptToMove.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'uid1', 'scriptToMove.js.map'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js'))).toBe(false)
+        expect(fileExistsSync(joinPath(outputPath, 'otherUID', 'scriptToIgnore.js.map'))).toBe(false)
       })
     })
   })
diff --git a/packages/app/src/cli/models/extensions/extension-instance.ts b/packages/app/src/cli/models/extensions/extension-instance.ts
index 074d27c5dd0..a39bd741ae8 100644
--- a/packages/app/src/cli/models/extensions/extension-instance.ts
+++ b/packages/app/src/cli/models/extensions/extension-instance.ts
@@ -27,7 +27,7 @@ import {ok} from '@shopify/cli-kit/node/result'
 import {constantize, slugify} from '@shopify/cli-kit/common/string'
 import {hashString, nonRandomUUID} from '@shopify/cli-kit/node/crypto'
 import {partnersFqdn} from '@shopify/cli-kit/node/context/fqdn'
-import {joinPath, basename, normalizePath, resolvePath} from '@shopify/cli-kit/node/path'
+import {joinPath, normalizePath, resolvePath, relativePath, basename} from '@shopify/cli-kit/node/path'
 import {fileExists, touchFile, moveFile, writeFile, glob, copyFile, globSync} from '@shopify/cli-kit/node/fs'
 import {getPathValue} from '@shopify/cli-kit/common/object'
 import {outputDebug} from '@shopify/cli-kit/node/output'
@@ -137,14 +137,11 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
   }
 
   get outputFileName() {
-    const mode = this.specification.buildConfig.mode
-    if (mode === 'copy_files' || mode === 'theme') {
-      return ''
-    } else if (mode === 'function') {
-      return 'index.wasm'
-    } else {
-      return `${this.handle}.js`
-    }
+    return basename(this.outputRelativePath)
+  }
+
+  get outputRelativePath() {
+    return this.specification.getOutputRelativePath?.(this) ?? ''
   }
 
   constructor(options: {
@@ -162,19 +159,9 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     this.handle = this.buildHandle()
     this.localIdentifier = this.handle
     this.idEnvironmentVariableName = `SHOPIFY_${constantize(this.localIdentifier)}_ID`
-    this.outputPath = this.directory
+    this.outputPath = joinPath(this.directory, this.outputRelativePath)
     this.uid = this.buildUIDFromStrategy()
     this.devUUID = `dev-${this.uid}`
-
-    if (this.features.includes('esbuild') || this.type === 'tax_calculation') {
-      this.outputPath = joinPath(this.directory, 'dist', this.outputFileName)
-    }
-
-    if (this.isFunctionExtension) {
-      const config = this.configuration as unknown as FunctionConfigType
-      const defaultPath = joinPath('dist', 'index.wasm')
-      this.outputPath = joinPath(this.directory, config.build?.path ?? defaultPath)
-    }
   }
 
   get draftMessages() {
@@ -247,7 +234,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     const pathToMove = pathsToMove[0]
     if (pathToMove === undefined) return Promise.resolve()
 
-    const outputPath = joinPath(this.directory, 'dist', basename(pathToMove))
+    const outputPath = joinPath(this.directory, relativePath(inputPath, pathToMove))
     await moveFile(pathToMove, outputPath, {overwrite: true})
     outputDebug(`Source map for ${this.localIdentifier} created: ${outputPath}`)
   }
@@ -408,8 +395,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
 
   getOutputPathForDirectory(directory: string, outputId?: string) {
     const id = this.getOutputFolderId(outputId)
-    const outputFile = this.outputFileName === '' ? '' : joinPath('dist', this.outputFileName)
-    return joinPath(directory, id, outputFile)
+    return joinPath(directory, id, this.outputRelativePath)
   }
 
   get singleTarget() {
diff --git a/packages/app/src/cli/models/extensions/specification.ts b/packages/app/src/cli/models/extensions/specification.ts
index 2f459524386..0ed780d6abc 100644
--- a/packages/app/src/cli/models/extensions/specification.ts
+++ b/packages/app/src/cli/models/extensions/specification.ts
@@ -72,6 +72,7 @@ export interface ExtensionSpecification<TConfiguration extends BaseConfigType =
   buildConfig: BuildConfig
   dependency?: string
   graphQLType?: string
+  getOutputRelativePath?: (extension: ExtensionInstance<TConfiguration>) => string
   getBundleExtensionStdinContent?: (config: TConfiguration) => {main: string; assets?: Asset[]}
   deployConfig?: (
     config: TConfiguration,
diff --git a/packages/app/src/cli/models/extensions/specifications/checkout_post_purchase.ts b/packages/app/src/cli/models/extensions/specifications/checkout_post_purchase.ts
index 616adf80b73..cbae1290736 100644
--- a/packages/app/src/cli/models/extensions/specifications/checkout_post_purchase.ts
+++ b/packages/app/src/cli/models/extensions/specifications/checkout_post_purchase.ts
@@ -1,9 +1,11 @@
+import {ExtensionInstance} from '../extension-instance.js'
 import {BaseSchema, MetafieldSchema} from '../schemas.js'
 import {createExtensionSpecification} from '../specification.js'
 import {zod} from '@shopify/cli-kit/node/schema'
 
 const dependency = '@shopify/post-purchase-ui-extensions'
 
+type CheckoutPostPurchaseConfigType = zod.infer<typeof CheckoutPostPurchaseSchema>
 const CheckoutPostPurchaseSchema = BaseSchema.extend({
   metafields: zod.array(MetafieldSchema).optional(),
 })
@@ -15,6 +17,8 @@ const checkoutPostPurchaseSpec = createExtensionSpecification({
   schema: CheckoutPostPurchaseSchema,
   appModuleFeatures: (_) => ['ui_preview', 'cart_url', 'esbuild', 'single_js_entry_path'],
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<CheckoutPostPurchaseConfigType>) =>
+    `dist/${extension.handle}.js`,
   deployConfig: async (config, _) => {
     return {metafields: config.metafields ?? []}
   },
diff --git a/packages/app/src/cli/models/extensions/specifications/checkout_ui_extension.ts b/packages/app/src/cli/models/extensions/specifications/checkout_ui_extension.ts
index f08dfd97c40..ab37ad6a44f 100644
--- a/packages/app/src/cli/models/extensions/specifications/checkout_ui_extension.ts
+++ b/packages/app/src/cli/models/extensions/specifications/checkout_ui_extension.ts
@@ -1,10 +1,12 @@
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema, MetafieldSchema} from '../schemas.js'
 import {loadLocalesConfig} from '../../../utilities/extensions/locales-configuration.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {zod} from '@shopify/cli-kit/node/schema'
 
 const dependency = '@shopify/checkout-ui-extensions'
 
+type CheckoutConfigType = zod.infer<typeof CheckoutSchema>
 const CheckoutSchema = BaseSchema.extend({
   name: zod.string(),
   extension_points: zod.array(zod.string()).optional(),
@@ -22,6 +24,7 @@ const checkoutSpec = createExtensionSpecification({
   schema: CheckoutSchema,
   appModuleFeatures: (_) => ['ui_preview', 'cart_url', 'esbuild', 'single_js_entry_path', 'generates_source_maps'],
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<CheckoutConfigType>) => `dist/${extension.handle}.js`,
   deployConfig: async (config, directory) => {
     return {
       extension_points: config.extension_points,
diff --git a/packages/app/src/cli/models/extensions/specifications/function.ts b/packages/app/src/cli/models/extensions/specifications/function.ts
index ce6d2ec5a5d..c1f80ee796e 100644
--- a/packages/app/src/cli/models/extensions/specifications/function.ts
+++ b/packages/app/src/cli/models/extensions/specifications/function.ts
@@ -1,6 +1,7 @@
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema} from '../schemas.js'
 import {loadLocalesConfig} from '../../../utilities/extensions/locales-configuration.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {zod} from '@shopify/cli-kit/node/schema'
 import {joinPath} from '@shopify/cli-kit/node/path'
 import {fileExists, readFile} from '@shopify/cli-kit/node/fs'
@@ -88,6 +89,8 @@ const functionSpec = createExtensionSpecification({
   schema: FunctionExtensionSchema,
   appModuleFeatures: (_) => ['function'],
   buildConfig: {mode: 'function'},
+  getOutputRelativePath: (extension: ExtensionInstance<FunctionConfigType>) =>
+    extension.configuration.build?.path ?? joinPath('dist', 'index.wasm'),
   deployConfig: async (config, directory, apiKey) => {
     let inputQuery: string | undefined
     const moduleId = randomUUID()
diff --git a/packages/app/src/cli/models/extensions/specifications/pos_ui_extension.ts b/packages/app/src/cli/models/extensions/specifications/pos_ui_extension.ts
index 33962306a24..2d9dc37b4ee 100644
--- a/packages/app/src/cli/models/extensions/specifications/pos_ui_extension.ts
+++ b/packages/app/src/cli/models/extensions/specifications/pos_ui_extension.ts
@@ -1,17 +1,22 @@
 import {getDependencyVersion} from '../../app/app.js'
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema} from '../schemas.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {BugError} from '@shopify/cli-kit/node/error'
 import {zod} from '@shopify/cli-kit/node/schema'
 
 const dependency = '@shopify/retail-ui-extensions'
 
+type PosUIConfigType = zod.infer<typeof PosUISchema>
+const PosUISchema = BaseSchema.extend({name: zod.string()})
+
 const posUISpec = createExtensionSpecification({
   identifier: 'pos_ui_extension',
   dependency,
-  schema: BaseSchema.extend({name: zod.string()}),
+  schema: PosUISchema,
   appModuleFeatures: (_) => ['ui_preview', 'esbuild', 'single_js_entry_path'],
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<PosUIConfigType>) => `dist/${extension.handle}.js`,
   deployConfig: async (config, directory) => {
     const result = await getDependencyVersion(dependency, directory)
     if (result === 'not_found') throw new BugError(`Dependency ${dependency} not found`)
diff --git a/packages/app/src/cli/models/extensions/specifications/product_subscription.ts b/packages/app/src/cli/models/extensions/specifications/product_subscription.ts
index ba807e409f6..2497a236130 100644
--- a/packages/app/src/cli/models/extensions/specifications/product_subscription.ts
+++ b/packages/app/src/cli/models/extensions/specifications/product_subscription.ts
@@ -1,10 +1,14 @@
 import {getDependencyVersion} from '../../app/app.js'
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema} from '../schemas.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {BugError} from '@shopify/cli-kit/node/error'
+import {zod} from '@shopify/cli-kit/node/schema'
 
 const dependency = '@shopify/admin-ui-extensions'
 
+type ProductSubscriptionConfigType = zod.infer<typeof BaseSchema>
+
 const productSubscriptionSpec = createExtensionSpecification({
   identifier: 'product_subscription',
   additionalIdentifiers: ['subscription_management'],
@@ -13,6 +17,7 @@ const productSubscriptionSpec = createExtensionSpecification({
   schema: BaseSchema,
   appModuleFeatures: (_) => ['ui_preview', 'esbuild', 'single_js_entry_path'],
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<ProductSubscriptionConfigType>) => `dist/${extension.handle}.js`,
   deployConfig: async (_, directory) => {
     const result = await getDependencyVersion(dependency, directory)
     if (result === 'not_found') throw new BugError(`Dependency ${dependency} not found`)
diff --git a/packages/app/src/cli/models/extensions/specifications/tax_calculation.ts b/packages/app/src/cli/models/extensions/specifications/tax_calculation.ts
index 1e97e577bb6..e7d09509939 100644
--- a/packages/app/src/cli/models/extensions/specifications/tax_calculation.ts
+++ b/packages/app/src/cli/models/extensions/specifications/tax_calculation.ts
@@ -1,11 +1,13 @@
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema, MetafieldSchema} from '../schemas.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {zod} from '@shopify/cli-kit/node/schema'
 
 const CartLinePropertySchema = zod.object({
   key: zod.string(),
 })
 
+type TaxCalculationsConfigType = zod.infer<typeof TaxCalculationsSchema>
 const TaxCalculationsSchema = BaseSchema.extend({
   production_api_base_url: zod.string(),
   benchmark_api_base_url: zod.string().optional(),
@@ -29,6 +31,7 @@ const spec = createExtensionSpecification({
   schema: TaxCalculationsSchema,
   appModuleFeatures: (_) => [],
   buildConfig: {mode: 'tax_calculation'},
+  getOutputRelativePath: (extension: ExtensionInstance<TaxCalculationsConfigType>) => `dist/${extension.handle}.js`,
   deployConfig: async (config, _) => {
     return {
       production_api_base_url: config.production_api_base_url,
diff --git a/packages/app/src/cli/models/extensions/specifications/ui_extension.ts b/packages/app/src/cli/models/extensions/specifications/ui_extension.ts
index f3e04cbeab9..8f8dc83d02a 100644
--- a/packages/app/src/cli/models/extensions/specifications/ui_extension.ts
+++ b/packages/app/src/cli/models/extensions/specifications/ui_extension.ts
@@ -36,6 +36,7 @@ export interface BuildManifest {
 
 const missingExtensionPointsMessage = 'No extension targets defined, add a `targeting` field to your configuration'
 
+type UIExtensionConfigType = zod.infer<typeof UIExtensionSchema>
 export const UIExtensionSchema = BaseSchema.extend({
   name: zod.string(),
   type: zod.literal('ui_extension'),
@@ -102,6 +103,7 @@ const uiExtensionSpec = createExtensionSpecification({
   dependency,
   schema: UIExtensionSchema,
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<UIExtensionConfigType>) => `dist/${extension.handle}.js`,
   appModuleFeatures: (config) => {
     const basic: ExtensionFeature[] = ['ui_preview', 'esbuild', 'generates_source_maps']
     const needsCart =
diff --git a/packages/app/src/cli/models/extensions/specifications/web_pixel_extension.ts b/packages/app/src/cli/models/extensions/specifications/web_pixel_extension.ts
index 298a18d876b..e512e66e5f4 100644
--- a/packages/app/src/cli/models/extensions/specifications/web_pixel_extension.ts
+++ b/packages/app/src/cli/models/extensions/specifications/web_pixel_extension.ts
@@ -1,5 +1,6 @@
 import {createExtensionSpecification} from '../specification.js'
 import {BaseSchema} from '../schemas.js'
+import {ExtensionInstance} from '../extension-instance.js'
 import {zod} from '@shopify/cli-kit/node/schema'
 import {AbortError} from '@shopify/cli-kit/node/error'
 import {fileSize} from '@shopify/cli-kit/node/fs'
@@ -10,6 +11,7 @@ const BUNDLE_SIZE_LIMIT = BUNDLE_SIZE_LIMIT_KB * kilobytes
 
 const dependency = '@shopify/web-pixels-extension'
 
+type WebPixelConfigType = zod.infer<typeof WebPixelSchema>
 const WebPixelSchema = BaseSchema.extend({
   runtime_context: zod.string(),
   version: zod.string().optional(),
@@ -32,6 +34,7 @@ const webPixelSpec = createExtensionSpecification({
   schema: WebPixelSchema,
   appModuleFeatures: (_) => ['esbuild', 'single_js_entry_path'],
   buildConfig: {mode: 'ui'},
+  getOutputRelativePath: (extension: ExtensionInstance<WebPixelConfigType>) => `dist/${extension.handle}.js`,
   deployConfig: async (config, _) => {
     return {
       runtime_context: config.runtime_context,
diff --git a/packages/app/src/cli/services/build/extension.ts b/packages/app/src/cli/services/build/extension.ts
index 21072a23f66..d1000080051 100644
--- a/packages/app/src/cli/services/build/extension.ts
+++ b/packages/app/src/cli/services/build/extension.ts
@@ -150,8 +150,7 @@ export async function buildFunctionExtension(
 
   try {
     const bundlePath = extension.outputPath
-    const relativeBuildPath =
-      (extension as ExtensionInstance<FunctionConfigType>).configuration.build?.path ?? joinPath('dist', 'index.wasm')
+    const relativeBuildPath = extension.specification.getOutputRelativePath?.(extension) ?? ''
 
     extension.outputPath = joinPath(extension.directory, relativeBuildPath)
 
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 7bf8116bc11..9cec5a369c4 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 {IncomingMessage, ServerResponse, sendRedirect, send} from 'h3'
-import {joinPath, extname, moduleDirectory} from '@shopify/cli-kit/node/path'
+import {joinPath, dirname, extname, moduleDirectory} from '@shopify/cli-kit/node/path'
 import {outputDebug} from '@shopify/cli-kit/node/output'
 
 export function corsMiddleware(_request: IncomingMessage, response: ServerResponse, next: (err?: Error) => unknown) {
@@ -90,7 +90,7 @@ export function getExtensionAssetMiddleware({devOptions, getExtensions}: GetExte
     const bundlePath = devOptions.appWatcher.buildOutputPath
     const extensionOutputPath = extension.getOutputPathForDirectory(bundlePath)
 
-    const buildDirectory = extensionOutputPath.replace(extension.outputFileName, '')
+    const buildDirectory = dirname(extensionOutputPath)
 
     return fileServerMiddleware(request, response, next, {
       filePath: joinPath(buildDirectory, assetPath),