diff --git a/packages/app/src/cli/models/app/loader.test.ts b/packages/app/src/cli/models/app/loader.test.ts
index a0a0222f9f..82ed6cf2ec 100644
--- a/packages/app/src/cli/models/app/loader.test.ts
+++ b/packages/app/src/cli/models/app/loader.test.ts
@@ -2768,9 +2768,8 @@ describe('WebhooksSchema', () => {
       ],
     }
     const errorObj = {
-      validation: 'regex' as zod.ZodInvalidStringIssue['validation'],
-      code: zod.ZodIssueCode.invalid_string,
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
+      code: zod.ZodIssueCode.custom,
+      message: "URI isn't correct URI format of https://, pubsub://{project-id}:{topic-id} or Eventbridge ARN",
       path: ['webhooks', 'subscriptions', 0, 'uri'],
     }
 
@@ -2796,9 +2795,8 @@ describe('WebhooksSchema', () => {
       subscriptions: [{uri: 'my::URI-thing::Shopify::123', topics: ['products/create']}],
     }
     const errorObj = {
-      validation: 'regex' as zod.ZodInvalidStringIssue['validation'],
-      code: zod.ZodIssueCode.invalid_string,
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
+      code: zod.ZodIssueCode.custom,
+      message: "URI isn't correct URI format of https://, pubsub://{project-id}:{topic-id} or Eventbridge ARN",
       path: ['webhooks', 'subscriptions', 0, 'uri'],
     }
 
@@ -2957,9 +2955,8 @@ describe('WebhooksSchema', () => {
       ],
     }
     const errorObj = {
-      validation: 'regex' as zod.ZodInvalidStringIssue['validation'],
-      code: zod.ZodIssueCode.invalid_string,
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
+      code: zod.ZodIssueCode.custom,
+      message: "URI isn't correct URI format of https://, pubsub://{project-id}:{topic-id} or Eventbridge ARN",
       path: ['webhooks', 'subscriptions', 0, 'uri'],
     }
 
diff --git a/packages/app/src/cli/models/app/loader.ts b/packages/app/src/cli/models/app/loader.ts
index b8975414f3..a76518ae90 100644
--- a/packages/app/src/cli/models/app/loader.ts
+++ b/packages/app/src/cli/models/app/loader.ts
@@ -284,6 +284,7 @@ class AppLoader<TConfig extends AppConfiguration, TModuleSpec extends ExtensionS
   private remoteFlags: Flag[]
   private dynamicallySpecifiedConfigs: DynamicallySpecifiedConfigLoading
   private loadedConfiguration: ConfigurationLoaderResult<TConfig, TModuleSpec>
+  private fullAppConfiguration?: CurrentAppConfiguration
 
   constructor(
     {mode, loadedConfiguration}: AppLoaderConstructorArgs<TConfig, TModuleSpec>,
@@ -298,6 +299,7 @@ class AppLoader<TConfig extends AppConfiguration, TModuleSpec extends ExtensionS
 
   async loaded() {
     const {configuration, directory, configurationLoadResultMetadata, configSchema} = this.loadedConfiguration
+    this.fullAppConfiguration = configuration as CurrentAppConfiguration
 
     await logMetadataFromAppLoadingProcess(configurationLoadResultMetadata)
 
@@ -463,6 +465,7 @@ class AppLoader<TConfig extends AppConfiguration, TModuleSpec extends ExtensionS
       entryPath,
       directory,
       specification,
+      fullAppConfiguration: this.fullAppConfiguration,
     })
 
     if (usedKnownSpecification) {
diff --git a/packages/app/src/cli/models/extensions/extension-instance.ts b/packages/app/src/cli/models/extensions/extension-instance.ts
index fc0ee13a99..dfe78a76e3 100644
--- a/packages/app/src/cli/models/extensions/extension-instance.ts
+++ b/packages/app/src/cli/models/extensions/extension-instance.ts
@@ -14,6 +14,7 @@ import {bundleThemeExtension} from '../../services/extensions/bundle.js'
 import {Identifiers} from '../app/identifiers.js'
 import {uploadWasmBlob} from '../../services/deploy/upload.js'
 import {DeveloperPlatformClient} from '../../utilities/developer-platform-client.js'
+import {CurrentAppConfiguration} from '../app/app.js'
 import {ok} from '@shopify/cli-kit/node/result'
 import {constantize, slugify} from '@shopify/cli-kit/common/string'
 import {hashString, randomUUID} from '@shopify/cli-kit/node/crypto'
@@ -47,6 +48,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
   handle: string
   specification: ExtensionSpecification
   uid: string
+  fullAppConfiguration?: CurrentAppConfiguration
 
   get graphQLType() {
     return (this.specification.graphQLType ?? this.specification.identifier).toUpperCase()
@@ -118,6 +120,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     entryPath?: string
     directory: string
     specification: ExtensionSpecification
+    fullAppConfiguration?: CurrentAppConfiguration
   }) {
     this.configuration = options.configuration
     this.configurationPath = options.configurationPath
@@ -130,6 +133,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     this.idEnvironmentVariableName = `SHOPIFY_${constantize(this.localIdentifier)}_ID`
     this.outputPath = this.directory
     this.uid = this.configuration.uid ?? randomUUID()
+    this.fullAppConfiguration = options.fullAppConfiguration
 
     if (this.features.includes('esbuild') || this.type === 'tax_calculation') {
       this.outputPath = joinPath(this.directory, 'dist', `${this.outputFileName}`)
@@ -186,9 +190,9 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
 
   async commonDeployConfig(apiKey: string): Promise<{[key: string]: unknown} | undefined> {
     const deployConfig = await this.specification.deployConfig?.(this.configuration, this.directory, apiKey, undefined)
-    const transformedConfig = this.specification.transformLocalToRemote?.(this.configuration) as
-      | {[key: string]: unknown}
-      | undefined
+    const transformedConfig = this.specification.transformLocalToRemote?.(this.configuration, {
+      fullAppConfiguration: this.fullAppConfiguration,
+    }) as {[key: string]: unknown} | undefined
     const resultDeployConfig = deployConfig ?? transformedConfig ?? undefined
     return resultDeployConfig && Object.keys(resultDeployConfig).length > 0 ? resultDeployConfig : undefined
   }
diff --git a/packages/app/src/cli/models/extensions/specification.ts b/packages/app/src/cli/models/extensions/specification.ts
index 1ff810948c..ff51349680 100644
--- a/packages/app/src/cli/models/extensions/specification.ts
+++ b/packages/app/src/cli/models/extensions/specification.ts
@@ -3,6 +3,7 @@ import {ExtensionInstance} from './extension-instance.js'
 import {blocks} from '../../constants.js'
 
 import {Flag} from '../../services/dev/fetch.js'
+import {CurrentAppConfiguration} from '../app/app.js'
 import {Result} from '@shopify/cli-kit/node/result'
 import {capitalize} from '@shopify/cli-kit/common/string'
 import {zod} from '@shopify/cli-kit/node/schema'
@@ -21,9 +22,13 @@ export interface TransformationConfig {
   [key: string]: string
 }
 
-export interface CustomTransformationConfig {
-  forward?: (obj: object, options?: {flags?: Flag[]}) => object
-  reverse?: (obj: object, options?: {flags?: Flag[]}) => object
+export interface CustomTransformationConfigOptions {
+  flags?: Flag[]
+  fullAppConfiguration?: CurrentAppConfiguration
+}
+export interface CustomTransformationConfig<T = object> {
+  forward?: (obj: T, options?: CustomTransformationConfigOptions) => object
+  reverse?: (obj: T, options?: CustomTransformationConfigOptions) => object
 }
 
 type ExtensionExperience = 'extension' | 'configuration'
@@ -64,7 +69,7 @@ export interface ExtensionSpecification<TConfiguration extends BaseConfigType =
    * @param localContent - Content taken from the local filesystem
    * @returns Transformed configuration to send to the platform in place of the locally provided content
    */
-  transformLocalToRemote?: (localContent: object) => object
+  transformLocalToRemote?: (localContent: object, options?: CustomTransformationConfigOptions) => object
 
   /**
    * If required, convert configuration from the platform to the format used locally in the filesystem.
@@ -73,7 +78,7 @@ export interface ExtensionSpecification<TConfiguration extends BaseConfigType =
    * @param options - Additional options to be used in the transformation
    * @returns Transformed configuration to use in place of the platform provided content
    */
-  transformRemoteToLocal?: (remoteContent: object, options?: {flags?: Flag[]}) => object
+  transformRemoteToLocal?: (remoteContent: object, options?: CustomTransformationConfigOptions) => object
 
   uidStrategy: UidStrategy
 }
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_privacy_compliance_webhooks.ts b/packages/app/src/cli/models/extensions/specifications/app_config_privacy_compliance_webhooks.ts
index 77acfac969..639161a021 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_privacy_compliance_webhooks.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_privacy_compliance_webhooks.ts
@@ -2,13 +2,18 @@ import {WebhookSubscription, WebhooksConfig} from './types/app_config_webhook.js
 import {WebhooksSchema} from './app_config_webhook_schemas/webhooks_schema.js'
 import {ComplianceTopic} from './app_config_webhook_schemas/webhook_subscription_schema.js'
 import {mergeAllWebhooks} from './transform/app_config_webhook.js'
-import {CustomTransformationConfig, createConfigExtensionSpecification} from '../specification.js'
+import {
+  CustomTransformationConfig,
+  CustomTransformationConfigOptions,
+  createConfigExtensionSpecification,
+} from '../specification.js'
 import {Flag} from '../../../services/dev/fetch.js'
 import {compact, getPathValue} from '@shopify/cli-kit/common/object'
 
 const PrivacyComplianceWebhooksTransformConfig: CustomTransformationConfig = {
-  forward: (content: object, _options?: {flags?: Flag[]}) => transformToPrivacyComplianceWebhooksModule(content),
-  reverse: (content: object, options?: {flags?: Flag[]}) =>
+  forward: (content: object, options?: CustomTransformationConfigOptions) =>
+    transformToPrivacyComplianceWebhooksModule(content, options),
+  reverse: (content: object, options?: CustomTransformationConfigOptions) =>
     transformFromPrivacyComplianceWebhooksModule(content, options),
 }
 
@@ -23,13 +28,14 @@ const appPrivacyComplienceSpec = createConfigExtensionSpecification({
 
 export default appPrivacyComplienceSpec
 
-function transformToPrivacyComplianceWebhooksModule(content: object) {
+function transformToPrivacyComplianceWebhooksModule(content: object, options?: CustomTransformationConfigOptions) {
   const webhooks = getPathValue(content, 'webhooks') as WebhooksConfig
+  const appUrl = options?.fullAppConfiguration?.application_url
 
   return compact({
-    customers_redact_url: getCustomersDeletionUri(webhooks),
-    customers_data_request_url: getCustomersDataRequestUri(webhooks),
-    shop_redact_url: getShopDeletionUri(webhooks),
+    customers_redact_url: relativeUri(getCustomersDeletionUri(webhooks), appUrl),
+    customers_data_request_url: relativeUri(getCustomersDataRequestUri(webhooks), appUrl),
+    shop_redact_url: relativeUri(getShopDeletionUri(webhooks), appUrl),
   })
 }
 
@@ -72,6 +78,10 @@ function getComplianceUri(webhooks: WebhooksConfig, complianceTopic: string): st
   return webhooks.subscriptions?.find((subscription) => subscription.compliance_topics?.includes(complianceTopic))?.uri
 }
 
+function relativeUri(uri?: string, appUrl?: string) {
+  return appUrl && uri?.startsWith('/') ? `${appUrl}${uri}` : uri
+}
+
 function getCustomersDeletionUri(webhooks: WebhooksConfig) {
   return getComplianceUri(webhooks, 'customers/redact') || webhooks?.privacy_compliance?.customer_deletion_url
 }
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_webhook.ts b/packages/app/src/cli/models/extensions/specifications/app_config_webhook.ts
index 2bc309dd9e..d9d48eb3f1 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_webhook.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_webhook.ts
@@ -1,11 +1,16 @@
 import {WebhooksSchema} from './app_config_webhook_schemas/webhooks_schema.js'
 import {transformToWebhookConfig, transformFromWebhookConfig} from './transform/app_config_webhook.js'
-import {CustomTransformationConfig, createConfigExtensionSpecification} from '../specification.js'
+import {
+  CustomTransformationConfig,
+  CustomTransformationConfigOptions,
+  createConfigExtensionSpecification,
+} from '../specification.js'
 
 export const WebhooksSpecIdentifier = 'webhooks'
 
 const WebhookTransformConfig: CustomTransformationConfig = {
-  forward: (content: object) => transformFromWebhookConfig(content),
+  forward: (content: object, options?: CustomTransformationConfigOptions) =>
+    transformFromWebhookConfig(content, options),
   reverse: (content: object) => transformToWebhookConfig(content),
 }
 
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.test.ts b/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.test.ts
index 3cc7bb5df9..8ac6591311 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.test.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.test.ts
@@ -1,4 +1,5 @@
 import spec from './app_config_webhook_subscription.js'
+import {CurrentAppConfiguration} from '../../app/app.js'
 import {describe, expect, test} from 'vitest'
 
 describe('webhook_subscription', () => {
@@ -80,4 +81,24 @@ describe('webhook_subscription', () => {
       })
     })
   })
+
+  describe('forwardTransform', () => {
+    test('when a relative URI is used, it inherits the application_url', () => {
+      const object = {
+        topics: ['products/create'],
+        uri: '/products',
+      }
+
+      const webhookSpec = spec
+
+      const result = webhookSpec.transformLocalToRemote!(object, {
+        fullAppConfiguration: {application_url: 'https://my-app-url.com'} as CurrentAppConfiguration,
+      })
+
+      expect(result).toEqual({
+        uri: 'https://my-app-url.com/products',
+        topics: ['products/create'],
+      })
+    })
+  })
 })
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.ts b/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.ts
index 9fa393b4ed..efd02a7dd5 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_webhook_subscription.ts
@@ -71,15 +71,22 @@ function transformToWebhookSubscriptionConfig(content: object) {
   }
 }
 
-const WebhookSubscriptionTransformConfig: CustomTransformationConfig = {
-  forward: (content: object) => content,
+type WebhookContent = zod.infer<typeof SingleWebhookSubscriptionSchema>
+const WebhookSubscriptionTransformConfig: CustomTransformationConfig<WebhookContent> = {
+  forward: ({uri, ...content}, options) => {
+    const appUrl = options?.fullAppConfiguration?.application_url
+    return {
+      uri: appUrl && uri.startsWith('/') ? `${appUrl}${uri}` : uri,
+      ...content,
+    }
+  },
   reverse: (content: object) => transformToWebhookSubscriptionConfig(content),
 }
 
 const appWebhookSubscriptionSpec = createConfigExtensionSpecification({
   identifier: WebhookSubscriptionSpecIdentifier,
   schema: SingleWebhookSubscriptionSchema,
-  transformConfig: WebhookSubscriptionTransformConfig,
+  transformConfig: WebhookSubscriptionTransformConfig as object,
   uidStrategy: 'dynamic',
 })
 
diff --git a/packages/app/src/cli/models/extensions/specifications/transform/app_config_webhook.ts b/packages/app/src/cli/models/extensions/specifications/transform/app_config_webhook.ts
index 3413411348..1b09faeb9b 100644
--- a/packages/app/src/cli/models/extensions/specifications/transform/app_config_webhook.ts
+++ b/packages/app/src/cli/models/extensions/specifications/transform/app_config_webhook.ts
@@ -1,17 +1,23 @@
+import {CustomTransformationConfigOptions} from '../../specification.js'
+import {SpecsAppConfiguration} from '../types/app_config.js'
 import {WebhooksConfig, NormalizedWebhookSubscription, WebhookSubscription} from '../types/app_config_webhook.js'
 import {deepCompare, deepMergeObjects, getPathValue} from '@shopify/cli-kit/common/object'
 
-export function transformFromWebhookConfig(content: object) {
+export function transformFromWebhookConfig(content: object, options?: CustomTransformationConfigOptions) {
   const webhooks = getPathValue(content, 'webhooks') as WebhooksConfig
   if (!webhooks) return content
 
   const webhookSubscriptions = []
   // eslint-disable-next-line @typescript-eslint/naming-convention
   const {api_version, subscriptions = []} = webhooks
+  const appUrl = (options?.fullAppConfiguration as unknown as SpecsAppConfiguration)?.application_url
 
   // Compliance topics are handled from app_config_privacy_compliance_webhooks.ts
   for (const {uri, topics, compliance_topics: _, ...optionalFields} of subscriptions) {
-    if (topics) webhookSubscriptions.push(topics.map((topic) => ({uri, topic, ...optionalFields})))
+    if (topics) {
+      const uriWithRelativePath = uri.startsWith('/') && appUrl ? `${appUrl}${uri}` : uri
+      webhookSubscriptions.push(topics.map((topic) => ({uri: uriWithRelativePath, topic, ...optionalFields})))
+    }
   }
 
   return webhookSubscriptions.length > 0 ? {subscriptions: webhookSubscriptions.flat(), api_version} : {api_version}
diff --git a/packages/app/src/cli/models/extensions/specifications/validation/common.ts b/packages/app/src/cli/models/extensions/specifications/validation/common.ts
index a7d0a0be5c..60268d67ba 100644
--- a/packages/app/src/cli/models/extensions/specifications/validation/common.ts
+++ b/packages/app/src/cli/models/extensions/specifications/validation/common.ts
@@ -10,17 +10,13 @@ const arnRegex =
 export const removeTrailingSlash = (arg: unknown) =>
   typeof arg === 'string' && arg.endsWith('/') ? arg.replace(/\/+$/, '') : arg
 
-export const UriValidation = zod.union(
-  [
-    zod.string({invalid_type_error: 'Value must be string'}).regex(httpsRegex, {
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
-    }),
-    zod.string({invalid_type_error: 'Value must be string'}).regex(pubSubRegex, {
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
-    }),
-    zod.string({invalid_type_error: 'Value must be string'}).regex(arnRegex, {
-      message: "URI isn't correct URI format of https://, pubsub://{project}:topic or Eventbridge ARN",
-    }),
-  ],
-  {invalid_type_error: 'Invalid URI format'},
+export const UriValidation = zod.string({invalid_type_error: 'Value must be string'}).refine(
+  (uri) => {
+    if (uri.startsWith('/')) return true
+
+    return httpsRegex.test(uri) || pubSubRegex.test(uri) || arnRegex.test(uri)
+  },
+  {
+    message: "URI isn't correct URI format of https://, pubsub://{project-id}:{topic-id} or Eventbridge ARN",
+  },
 )
diff --git a/packages/app/src/cli/services/app/config/link.test.ts b/packages/app/src/cli/services/app/config/link.test.ts
index 913eefafb9..25cefb48d4 100644
--- a/packages/app/src/cli/services/app/config/link.test.ts
+++ b/packages/app/src/cli/services/app/config/link.test.ts
@@ -1128,7 +1128,7 @@ redirect_urls = [ "https://example.com/callback1" ]
 api_version = "2023-07"
 
   [[webhooks.subscriptions]]
-  uri = "https://example.com/customers"
+  uri = "/customers"
   compliance_topics = [ "customers/redact", "customers/data_request" ]
 
 [pos]
@@ -1171,13 +1171,139 @@ embedded = false
         subscriptions: [
           {
             compliance_topics: ['customers/redact', 'customers/data_request'],
-            uri: 'https://example.com/customers',
+            uri: '/customers',
+          },
+        ],
+      },
+      pos: {
+        embedded: false,
+      },
+      path: expect.stringMatching(/\/shopify.app.toml$/),
+    })
+    expect(content).toEqual(expectedContent)
+  })
+})
+
+test('simplifies the webhook config using relative paths', async () => {
+  await inTemporaryDirectory(async (tmp) => {
+    // Given
+    const developerPlatformClient = testDeveloperPlatformClient({
+      appExtensionRegistrations: (_app: MinimalAppIdentifiers) => Promise.resolve(remoteExtensionRegistrations),
+    })
+    const remoteExtensionRegistrations = {
+      app: {
+        extensionRegistrations: [],
+        configurationRegistrations: [
+          {
+            type: 'WEBHOOK_SUBSCRIPTION',
+            id: '123',
+            uuid: '123',
+            title: 'Webhook subscription',
+            activeVersion: {
+              config: JSON.stringify({
+                api_version: '2024-01',
+                topic: 'products/create',
+                uri: 'https://my-app-url.com/webhooks',
+              }),
+            },
+          },
+          {
+            type: 'WEBHOOK_SUBSCRIPTION',
+            id: '1234',
+            uuid: '1234',
+            title: 'Webhook subscription',
+            activeVersion: {
+              config: JSON.stringify({
+                api_version: '2024-01',
+                topic: 'products/update',
+                uri: 'https://my-app-url.com/webhooks',
+              }),
+            },
+          },
+        ],
+        dashboardManagedExtensionRegistrations: [],
+      },
+    }
+    const options: LinkOptions = {
+      directory: tmp,
+      developerPlatformClient,
+    }
+
+    vi.mocked(fetchOrCreateOrganizationApp).mockResolvedValue(mockRemoteApp({developerPlatformClient}))
+    const remoteConfiguration = {
+      ...DEFAULT_REMOTE_CONFIGURATION,
+      application_url: 'https://my-app-url.com',
+      webhooks: {
+        api_version: '2023-07',
+        subscriptions: [
+          {
+            topics: ['products/create'],
+            uri: 'https://my-app-url.com/webhooks',
+          },
+          {
+            topics: ['products/update'],
+            uri: 'https://my-app-url.com/webhooks',
+          },
+        ],
+      },
+    }
+    vi.mocked(fetchAppRemoteConfiguration).mockResolvedValue(remoteConfiguration)
+
+    // When
+    const configuration = await link(options)
+
+    // Then
+    const content = await readFile(joinPath(tmp, 'shopify.app.toml'))
+    const expectedContent = `# Learn more about configuring your app at https://shopify.dev/docs/apps/tools/cli/configuration
+
+client_id = "12345"
+name = "app1"
+application_url = "https://my-app-url.com"
+embedded = true
+
+[access_scopes]
+# Learn more at https://shopify.dev/docs/apps/tools/cli/configuration#access_scopes
+use_legacy_install_flow = true
+
+[auth]
+redirect_urls = [ "https://example.com/callback1" ]
+
+[webhooks]
+api_version = "2023-07"
+
+  [[webhooks.subscriptions]]
+  topics = [ "products/create", "products/update" ]
+  uri = "/webhooks"
+
+[pos]
+embedded = false
+`
+
+    expect(configuration).toEqual({
+      client_id: '12345',
+      name: 'app1',
+      application_url: 'https://my-app-url.com',
+      embedded: true,
+      access_scopes: {
+        use_legacy_install_flow: true,
+      },
+      build: undefined,
+      auth: {
+        redirect_urls: ['https://example.com/callback1'],
+      },
+      webhooks: {
+        api_version: '2023-07',
+        subscriptions: [
+          {
+            topics: ['products/create', 'products/update'],
+            uri: '/webhooks',
           },
         ],
       },
       pos: {
         embedded: false,
       },
+      scopes: undefined,
       path: expect.stringMatching(/\/shopify.app.toml$/),
     })
     expect(content).toEqual(expectedContent)
diff --git a/packages/app/src/cli/services/app/config/link.ts b/packages/app/src/cli/services/app/config/link.ts
index bdc084c3ea..8c74838460 100644
--- a/packages/app/src/cli/services/app/config/link.ts
+++ b/packages/app/src/cli/services/app/config/link.ts
@@ -33,7 +33,6 @@ import {SpecsAppConfiguration} from '../../../models/extensions/specifications/t
 import {getTomls} from '../../../utilities/app/config/getTomls.js'
 import {loadLocalExtensionsSpecifications} from '../../../models/extensions/load-specifications.js'
 import {reduceWebhooks} from '../../../models/extensions/specifications/transform/app_config_webhook.js'
-import {WebhooksConfig} from '../../../models/extensions/specifications/types/app_config_webhook.js'
 import {renderSuccess} from '@shopify/cli-kit/node/ui'
 import {formatPackageManagerCommand} from '@shopify/cli-kit/node/output'
 import {deepMergeObjects, isEmpty} from '@shopify/cli-kit/common/object'
@@ -333,13 +332,18 @@ async function loadConfigurationFileName(
  * but when we link we want to condense all webhooks together
  * so we have to do an additional reduce here
  */
-function condenseComplianceAndNonComplianceWebhooks(config: {[key: string]: unknown}): CurrentAppConfiguration {
-  const webhooksConfig = (config.webhooks as WebhooksConfig) ?? {}
-  if (webhooksConfig.subscriptions?.length) {
+function condenseComplianceAndNonComplianceWebhooks(config: CurrentAppConfiguration) {
+  const webhooksConfig = config.webhooks
+  if (webhooksConfig?.subscriptions?.length) {
+    const appUrl = config?.application_url as string | undefined
     webhooksConfig.subscriptions = reduceWebhooks(webhooksConfig.subscriptions)
+    webhooksConfig.subscriptions = webhooksConfig.subscriptions.map(({uri, ...subscription}) => ({
+      uri: appUrl && uri.includes(appUrl) ? uri.replace(appUrl, '') : uri,
+      ...subscription,
+    }))
   }
 
-  return config as unknown as CurrentAppConfiguration
+  return config
 }
 
 /**
diff --git a/packages/app/src/cli/utilities/extensions/configuration.ts b/packages/app/src/cli/utilities/extensions/configuration.ts
index 43edc1a00b..aba2f442a5 100644
--- a/packages/app/src/cli/utilities/extensions/configuration.ts
+++ b/packages/app/src/cli/utilities/extensions/configuration.ts
@@ -2,7 +2,6 @@ interface GetUIExensionResourceURLOptions {
   checkoutCartUrl?: string
   subscriptionProductUrl?: string
 }
-
 export function getUIExtensionResourceURL(
   uiExtensionType: string,
   options: GetUIExensionResourceURLOptions,