diff --git a/packages/app/src/cli/models/app/loader.test.ts b/packages/app/src/cli/models/app/loader.test.ts
index fcd9174262..010b50df6e 100644
--- a/packages/app/src/cli/models/app/loader.test.ts
+++ b/packages/app/src/cli/models/app/loader.test.ts
@@ -2350,9 +2350,8 @@ describe('WebhooksSchema', () => {
       ],
     }
     const errorObj = {
-      validation: 'regex' as zod.ZodInvalidStringIssue['validation'],
-      code: zod.ZodIssueCode.invalid_string,
-      message: 'Invalid',
+      code: zod.ZodIssueCode.custom,
+      message: 'Must be a valid https, pubsub, or ARN URI',
       path: ['webhooks', 'subscriptions', 0, 'uri'],
     }
 
@@ -2378,9 +2377,8 @@ 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: 'Invalid',
+      code: zod.ZodIssueCode.custom,
+      message: 'Must be a valid https, pubsub, or ARN URI',
       path: ['webhooks', 'subscriptions', 0, 'uri'],
     }
 
@@ -2426,6 +2424,22 @@ describe('WebhooksSchema', () => {
     expect(parsedConfiguration.webhooks).toMatchObject(webhookConfig)
   })
 
+  test('accepts a relative path uri', async () => {
+    const webhookConfig: WebhooksConfig = {
+      api_version: '2021-07',
+      subscriptions: [
+        {
+          uri: '/webhooks',
+          topics: ['products/create'],
+        },
+      ],
+    }
+
+    const {abortOrReport, parsedConfiguration} = await setupParsing({}, webhookConfig)
+    expect(abortOrReport).not.toHaveBeenCalled()
+    expect(parsedConfiguration.webhooks).toMatchObject(webhookConfig)
+  })
+
   test('accepts combination of uris', async () => {
     const webhookConfig: WebhooksConfig = {
       api_version: '2021-07',
@@ -2442,6 +2456,10 @@ describe('WebhooksSchema', () => {
           uri: 'pubsub://my-project-123:my-topic',
           topics: ['products/create', 'products/update'],
         },
+        {
+          uri: '/webhooks',
+          topics: ['products/create', 'products/update'],
+        },
       ],
     }
 
@@ -2531,9 +2549,8 @@ describe('WebhooksSchema', () => {
       ],
     }
     const errorObj = {
-      validation: 'regex' as zod.ZodInvalidStringIssue['validation'],
-      code: zod.ZodIssueCode.invalid_string,
-      message: 'Invalid',
+      code: zod.ZodIssueCode.custom,
+      message: 'Must be a valid https, pubsub, or ARN URI',
       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 cb32f2b7be..fa38d0e500 100644
--- a/packages/app/src/cli/models/app/loader.ts
+++ b/packages/app/src/cli/models/app/loader.ts
@@ -191,6 +191,7 @@ class AppLoader {
   private errors: AppErrors = new AppErrors()
   private specifications: ExtensionSpecification[]
   private remoteBetas: BetaFlag[]
+  private fullAppConfiguration?: AppConfiguration
 
   constructor({directory, configName, mode, specifications, remoteBetas}: AppLoaderConstructorArgs) {
     this.mode = mode ?? 'strict'
@@ -220,6 +221,7 @@ class AppLoader {
       specifications: this.specifications,
     })
     const {directory, configuration, configurationLoadResultMetadata, configSchema} = await configurationLoader.loaded()
+    this.fullAppConfiguration = configuration
     await logMetadataFromAppLoadingProcess(configurationLoadResultMetadata)
 
     const dotenv = await loadDotEnv(directory, configuration.path)
@@ -334,6 +336,7 @@ class AppLoader {
       entryPath,
       directory,
       specification,
+      fullAppConfig: this.fullAppConfiguration,
     })
 
     const validateResult = await extensionInstance.validate()
diff --git a/packages/app/src/cli/models/extensions/extension-instance.ts b/packages/app/src/cli/models/extensions/extension-instance.ts
index 31014769da..388f3ef6a2 100644
--- a/packages/app/src/cli/models/extensions/extension-instance.ts
+++ b/packages/app/src/cli/models/extensions/extension-instance.ts
@@ -10,6 +10,7 @@ import {
 import {bundleThemeExtension} from '../../services/extensions/bundle.js'
 import {Identifiers} from '../app/identifiers.js'
 import {uploadWasmBlob} from '../../services/deploy/upload.js'
+import {AppConfiguration} from '../app/app.js'
 import {ok} from '@shopify/cli-kit/node/result'
 import {constantize, slugify} from '@shopify/cli-kit/common/string'
 import {randomUUID} from '@shopify/cli-kit/node/crypto'
@@ -42,6 +43,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
   outputPath: string
   handle: string
   specification: ExtensionSpecification
+  fullAppConfiguration?: AppConfiguration
 
   get graphQLType() {
     return (this.specification.graphQLType ?? this.specification.identifier).toUpperCase()
@@ -109,6 +111,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     entryPath?: string
     directory: string
     specification: ExtensionSpecification
+    fullAppConfig?: AppConfiguration
   }) {
     this.configuration = options.configuration
     this.configurationPath = options.configurationPath
@@ -123,6 +126,7 @@ export class ExtensionInstance<TConfiguration extends BaseConfigType = BaseConfi
     this.localIdentifier = this.handle
     this.idEnvironmentVariableName = `SHOPIFY_${constantize(this.localIdentifier)}_ID`
     this.outputPath = this.directory
+    this.fullAppConfiguration = options.fullAppConfig
 
     if (this.features.includes('esbuild') || this.type === 'tax_calculation') {
       this.outputPath = joinPath(this.directory, 'dist', `${this.outputFileName}`)
@@ -175,7 +179,9 @@ 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.transform?.(this.configuration) as {[key: string]: unknown} | undefined
+    const transformedConfig = this.specification.transform?.(this.configuration, 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 3bc08d7043..89f5b094c5 100644
--- a/packages/app/src/cli/models/extensions/specification.ts
+++ b/packages/app/src/cli/models/extensions/specification.ts
@@ -21,7 +21,7 @@ export interface TransformationConfig {
 }
 
 export interface CustomTransformationConfig {
-  forward?: (obj: object) => object
+  forward?: (obj: object, fullAppConfiguration?: object) => object
   reverse?: (obj: object) => object
 }
 
@@ -55,8 +55,8 @@ export interface ExtensionSpecification<TConfiguration extends BaseConfigType =
   buildValidation?: (extension: ExtensionInstance<TConfiguration>) => Promise<void>
   hasExtensionPointTarget?(config: TConfiguration, target: string): boolean
   appModuleFeatures: (config?: TConfiguration) => ExtensionFeature[]
-  transform?: (content: object) => object
-  reverseTransform?: (content: object) => object
+  transform?: (content: object, fullAppConfiguration?: object) => object
+  reverseTransform?: (content: object, fullAppConfiguration?: object) => object
 }
 
 /**
diff --git a/packages/app/src/cli/models/extensions/specifications/app_config_webhook.test.ts b/packages/app/src/cli/models/extensions/specifications/app_config_webhook.test.ts
index 02b4d46f1a..fd9929cbcc 100644
--- a/packages/app/src/cli/models/extensions/specifications/app_config_webhook.test.ts
+++ b/packages/app/src/cli/models/extensions/specifications/app_config_webhook.test.ts
@@ -126,6 +126,39 @@ describe('webhooks', () => {
         api_version: '2021-01',
       })
     })
+    test('when a relative URI is used, it inherits the application_url', () => {
+      // Given
+      const object = {
+        webhooks: {
+          api_version: '2021-01',
+          subscriptions: [
+            {
+              topics: ['products/update', 'products/delete'],
+              uri: '/products',
+            },
+          ],
+        },
+      }
+      const webhookSpec = spec
+
+      // When
+      const result = webhookSpec.transform!(object, {application_url: 'https://my-app-url.com'})
+
+      // Then
+      expect(result).toEqual({
+        api_version: '2021-01',
+        subscriptions: [
+          {
+            topic: 'products/update',
+            uri: 'https://my-app-url.com/products',
+          },
+          {
+            topic: 'products/delete',
+            uri: 'https://my-app-url.com/products',
+          },
+        ],
+      })
+    })
   })
   describe('reverseTransform', () => {
     test('should return the reversed transformed object', () => {
@@ -246,5 +279,62 @@ describe('webhooks', () => {
         },
       })
     })
+    test('when subscriptions share the application_url base, simplify with a relative path', () => {
+      // Given
+      const object = {
+        api_version: '2021-01',
+        subscriptions: [
+          {
+            topic: 'products/update',
+            uri: 'https://my-app-url.com/products',
+          },
+          {
+            topic: 'products/delete',
+            uri: 'https://my-app-url.com/products',
+          },
+          {
+            topic: 'orders/update',
+            uri: 'https://my-app-url.com/orders',
+          },
+          {
+            topic: 'customers/create',
+            uri: 'https://customers-url.com',
+          },
+          {
+            topic: 'customers/delete',
+            uri: 'pubsub://absolute-feat-test:pub-sub-topic',
+          },
+        ],
+      }
+      const webhookSpec = spec
+
+      // When
+      const result = webhookSpec.reverseTransform!(object, {application_url: 'https://my-app-url.com'})
+
+      // Then
+      expect(result).toMatchObject({
+        webhooks: {
+          api_version: '2021-01',
+          subscriptions: [
+            {
+              topics: ['products/update', 'products/delete'],
+              uri: '/products',
+            },
+            {
+              topics: ['orders/update'],
+              uri: '/orders',
+            },
+            {
+              topics: ['customers/create'],
+              uri: 'https://customers-url.com',
+            },
+            {
+              topics: ['customers/delete'],
+              uri: 'pubsub://absolute-feat-test:pub-sub-topic',
+            },
+          ],
+        },
+      })
+    })
   })
 })
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 2f619c3159..19808e8b60 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
@@ -25,7 +25,7 @@ const WebhooksSchema = zod.object({
   subscriptions: zod.array(WebhookSubscriptionSchema).optional(),
 })
 
-export const WebhooksSchemaWithDeclarative = WebhooksSchema.superRefine(webhookValidator)
+const WebhooksSchemaWithDeclarative = WebhooksSchema.superRefine(webhookValidator)
 
 export const WebhookSchema = zod.object({
   webhooks: WebhooksSchemaWithDeclarative,
@@ -34,8 +34,8 @@ export const WebhookSchema = zod.object({
 export const WebhooksSpecIdentifier = 'webhooks'
 
 const WebhookTransformConfig: CustomTransformationConfig = {
-  forward: (content: object) => transformWebhookConfig(content),
-  reverse: (content: object) => transformToWebhookConfig(content),
+  forward: transformWebhookConfig,
+  reverse: transformToWebhookConfig,
 }
 
 const spec = createConfigExtensionSpecification({
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 97c4a87977..bf98974a7c 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
@@ -1,10 +1,14 @@
+import {SpecsAppConfiguration} from '../types/app_config.js'
 import {WebhooksConfig, NormalizedWebhookSubscription} from '../types/app_config_webhook.js'
 import {deepMergeObjects, getPathValue} from '@shopify/cli-kit/common/object'
 
-export function transformWebhookConfig(content: object) {
+export function transformWebhookConfig(content: object, fullAppConfig?: object) {
   const webhooks = getPathValue(content, 'webhooks') as WebhooksConfig
   if (!webhooks) return content
 
+  const appConfig = fullAppConfig as SpecsAppConfiguration
+  const applicationUrl = appConfig?.application_url
+
   const webhookSubscriptions = []
   // eslint-disable-next-line @typescript-eslint/naming-convention
   const {api_version, subscriptions = []} = webhooks
@@ -12,13 +16,14 @@ export function transformWebhookConfig(content: object) {
   // eslint-disable-next-line no-warning-comments
   // TODO: pass along compliance_topics once we're ready to store them in its own module
   for (const {uri, topics, compliance_topics: _, ...optionalFields} of subscriptions) {
-    webhookSubscriptions.push(topics.map((topic) => ({uri, topic, ...optionalFields})))
+    const uriWithRelativePath = uri.startsWith('/') && applicationUrl ? `${applicationUrl}${uri}` : uri
+    webhookSubscriptions.push(topics.map((topic) => ({uri: uriWithRelativePath, topic, ...optionalFields})))
   }
 
   return webhookSubscriptions.length > 0 ? {subscriptions: webhookSubscriptions.flat(), api_version} : {api_version}
 }
 
-export function transformToWebhookConfig(content: object) {
+export function transformToWebhookConfig(content: object, fullAppConfig?: object) {
   let webhooks = {}
   const apiVersion = getPathValue(content, 'api_version') as string
   webhooks = {...(apiVersion ? {webhooks: {api_version: apiVersion}} : {})}
@@ -27,15 +32,22 @@ export function transformToWebhookConfig(content: object) {
 
   const webhooksSubscriptions: WebhooksConfig['subscriptions'] = []
 
+  const appConfig = fullAppConfig as SpecsAppConfiguration
+  const applicationUrl = appConfig?.application_url
+
   // eslint-disable-next-line @typescript-eslint/naming-convention
   for (const {uri, topic, sub_topic, ...optionalFields} of serverWebhooks) {
-    const currSubscription = webhooksSubscriptions.find((sub) => sub.uri === uri && sub.sub_topic === sub_topic)
+    const uriWithRelativePath = uri.includes(applicationUrl) ? uri.replace(applicationUrl, '') : uri
+
+    const currSubscription = webhooksSubscriptions.find(
+      (sub) => sub.uri === uriWithRelativePath && sub.sub_topic === sub_topic,
+    )
     if (currSubscription) {
       currSubscription.topics.push(topic)
     } else {
       webhooksSubscriptions.push({
         topics: [topic],
-        uri,
+        uri: uriWithRelativePath,
         ...(sub_topic ? {sub_topic} : {}),
         ...optionalFields,
       })
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 fc3db473cb..169bdb67cb 100644
--- a/packages/app/src/cli/models/extensions/specifications/validation/common.ts
+++ b/packages/app/src/cli/models/extensions/specifications/validation/common.ts
@@ -15,8 +15,13 @@ export const ensureHttpsOnlyUrl = validateUrl(zod.string(), {
   message: 'Only https urls are allowed',
 }).refine((url) => !url.endsWith('/'), {message: 'URL can’t end with a forward slash'})
 
-export const UriValidation = zod.union([
-  zod.string().regex(httpsRegex),
-  zod.string().regex(pubSubRegex),
-  zod.string().regex(arnRegex),
-])
+export const UriValidation = zod.string().refine(
+  (uri) => {
+    if (uri.startsWith('/')) return true
+
+    return httpsRegex.test(uri) || pubSubRegex.test(uri) || arnRegex.test(uri)
+  },
+  {
+    message: 'Must be a valid https, pubsub, or ARN URI',
+  },
+)
diff --git a/packages/app/src/cli/services/app/select-app.ts b/packages/app/src/cli/services/app/select-app.ts
index 4811e7ff6d..53df5925ae 100644
--- a/packages/app/src/cli/services/app/select-app.ts
+++ b/packages/app/src/cli/services/app/select-app.ts
@@ -47,7 +47,10 @@ export function remoteAppConfigurationExtensionContent(
     if (!configString) return
     const config = configString ? JSON.parse(configString) : {}
 
-    remoteAppConfig = deepMergeObjects(remoteAppConfig, configSpec.reverseTransform?.(config) ?? config)
+    remoteAppConfig = deepMergeObjects(
+      remoteAppConfig,
+      configSpec.reverseTransform?.(config, remoteAppConfig) ?? config,
+    )
   })
   return {...remoteAppConfig}
 }