diff --git a/packages/app/src/cli/models/app/loader.test.ts b/packages/app/src/cli/models/app/loader.test.ts
index b5704a8692..a84b78c56e 100644
--- a/packages/app/src/cli/models/app/loader.test.ts
+++ b/packages/app/src/cli/models/app/loader.test.ts
@@ -31,10 +31,11 @@ import {
 import {inTemporaryDirectory, moveFile, mkdir, mkTmpDir, rmdir, writeFile} from '@shopify/cli-kit/node/fs'
 import {joinPath, dirname, cwd, normalizePath} from '@shopify/cli-kit/node/path'
 import {platformAndArch} from '@shopify/cli-kit/node/os'
-import {outputContent} from '@shopify/cli-kit/node/output'
+import {outputContent, outputToken} from '@shopify/cli-kit/node/output'
 import {zod} from '@shopify/cli-kit/node/schema'
 import {mockAndCaptureOutput} from '@shopify/cli-kit/node/testing/output'
 import {currentProcessIsGlobal} from '@shopify/cli-kit/node/is-global'
+import colors from '@shopify/cli-kit/node/colors'
 // eslint-disable-next-line no-restricted-imports
 import {resolve} from 'path'
 
@@ -417,7 +418,7 @@ wrong = "property"
     })
 
     // When
-    await expect(loadTestingApp()).rejects.toThrow(/Validation errors in/)
+    await expect(loadTestingApp()).rejects.toThrow(/Validation errors/)
   })
 
   test('throws an error if the extension type is invalid', async () => {
@@ -2483,9 +2484,9 @@ describe('parseConfigurationObject', () => {
         message: 'Boolean is required',
       },
     ]
-    const expectedFormatted = outputContent`App configuration is not valid\nValidation errors in tmp:\n\n${parseHumanReadableError(
-      errorObject,
-    )}`
+    const expectedFormatted = outputContent`\n${outputToken.errorText(
+      'Validation errors',
+    )} in tmp:\n\n${parseHumanReadableError(errorObject)}`
 
     const abortOrReport = vi.fn()
 
@@ -2510,9 +2511,9 @@ describe('parseConfigurationObject', () => {
         message: 'Expected string, received array',
       },
     ]
-    const expectedFormatted = outputContent`App configuration is not valid\nValidation errors in tmp:\n\n${parseHumanReadableError(
-      errorObject,
-    )}`
+    const expectedFormatted = outputContent`\n${outputToken.errorText(
+      'Validation errors',
+    )} in tmp:\n\n${parseHumanReadableError(errorObject)}`
     const abortOrReport = vi.fn()
     await parseConfigurationObject(LegacyAppSchema, 'tmp', configurationObject, abortOrReport)
 
@@ -2559,9 +2560,9 @@ describe('parseConfigurationObject', () => {
         message: 'Invalid input',
       },
     ]
-    const expectedFormatted = outputContent`App configuration is not valid\nValidation errors in tmp:\n\n${parseHumanReadableError(
-      errorObject,
-    )}`
+    const expectedFormatted = outputContent`\n${outputToken.errorText(
+      'Validation errors',
+    )} in tmp:\n\n${parseHumanReadableError(errorObject)}`
     const abortOrReport = vi.fn()
     await parseConfigurationObject(WebConfigurationSchema, 'tmp', configurationObject, abortOrReport)
 
@@ -2712,16 +2713,14 @@ describe('WebhooksSchema', () => {
   test('throws an error if we have duplicate subscriptions in same topics array', async () => {
     const webhookConfig: WebhooksConfig = {
       api_version: '2021-07',
-      subscriptions: [
-        {uri: 'https://example.com', topics: ['products/create', 'products/create']},
-        {uri: 'https://example.com', topics: ['products/create']},
-      ],
+      subscriptions: [{uri: 'https://example.com', topics: ['products/create', 'products/create']}],
     }
+    const webhookFields = colors.dim(`\n\ntopic: products/create\nuri: https://example.com`)
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/create'],
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2736,11 +2735,12 @@ describe('WebhooksSchema', () => {
         {uri: 'https://example.com', topics: ['products/create', 'products/update']},
       ],
     }
+    const webhookFields = colors.dim(`\n\ntopic: products/create\nuri: https://example.com`)
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/create'],
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2814,11 +2814,12 @@ describe('WebhooksSchema', () => {
         },
       ],
     }
+    const webhookFields = colors.dim(`\n\ntopic: products/create\nuri: https://example.com`)
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/create'],
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2839,11 +2840,12 @@ describe('WebhooksSchema', () => {
         },
       ],
     }
+    const webhookFields = colors.dim(`\n\ntopic: products/create\nuri: pubsub://my-project-123:my-topic`)
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/create'],
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2864,11 +2866,14 @@ describe('WebhooksSchema', () => {
         },
       ],
     }
+    const webhookFields = colors.dim(
+      `\n\ntopic: products/create\nuri: arn:aws:events:us-west-2::event-source/aws.partner/shopify.com/123/my_webhook_path`,
+    )
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/create'],
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2891,11 +2896,50 @@ describe('WebhooksSchema', () => {
         },
       ],
     }
+    const webhookFields = colors.dim(`\n\ntopic: products/update\nuri: https://example.com\nfilter: title:shoes`)
     const errorObj = {
       code: zod.ZodIssueCode.custom,
-      message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
       fatal: true,
-      path: ['webhooks', 'subscriptions', 1, 'topics', 0, 'products/update'],
+      path: ['webhooks', 'subscriptions'],
+    }
+
+    const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
+    expect(abortOrReport).toHaveBeenCalledWith(expectedFormatted, {}, 'tmp')
+  })
+
+  test('shows multiple duplicate subscriptions in error message', async () => {
+    const webhookConfig: WebhooksConfig = {
+      api_version: '2021-07',
+      subscriptions: [
+        {
+          topics: ['products/update'],
+          uri: 'https://example.com',
+          filter: 'title:shoes',
+        },
+        {
+          topics: ['products/update'],
+          uri: 'https://example.com',
+          filter: 'title:shoes',
+        },
+        {
+          topics: ['products/create'],
+          uri: 'https://example.com',
+        },
+        {
+          topics: ['products/create'],
+          uri: 'https://example.com',
+        },
+      ],
+    }
+    const webhookFields =
+      colors.dim(`\n\ntopic: products/update\nuri: https://example.com\nfilter: title:shoes`) +
+      colors.dim(`\n\ntopic: products/create\nuri: https://example.com`)
+    const errorObj = {
+      code: zod.ZodIssueCode.custom,
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${webhookFields}`,
+      fatal: true,
+      path: ['webhooks', 'subscriptions'],
     }
 
     const {abortOrReport, expectedFormatted} = await setupParsing(errorObj, webhookConfig)
@@ -2993,9 +3037,9 @@ describe('WebhooksSchema', () => {
 
   async function setupParsing(errorObj: zod.ZodIssue | {}, webhookConfigOverrides: WebhooksConfig) {
     const err = Array.isArray(errorObj) ? errorObj : [errorObj]
-    const expectedFormatted = outputContent`App configuration is not valid\nValidation errors in tmp:\n\n${parseHumanReadableError(
-      err,
-    )}`
+    const expectedFormatted = outputContent`\n${outputToken.errorText(
+      'Validation errors',
+    )} in tmp:\n\n${parseHumanReadableError(err)}`
     const abortOrReport = vi.fn()
 
     const {path, ...toParse} = getWebhookConfig(webhookConfigOverrides)
diff --git a/packages/app/src/cli/models/app/loader.ts b/packages/app/src/cli/models/app/loader.ts
index 36c1350b81..3db353645b 100644
--- a/packages/app/src/cli/models/app/loader.ts
+++ b/packages/app/src/cli/models/app/loader.ts
@@ -137,7 +137,7 @@ export function parseConfigurationObject<TSchema extends zod.ZodType>(
   const parseResult = schema.safeParse(configurationObject)
   if (!parseResult.success) {
     return abortOrReport(
-      outputContent`App configuration is not valid\nValidation errors in ${outputToken.path(
+      outputContent`\n${outputToken.errorText('Validation errors')} in ${outputToken.path(
         filepath,
       )}:\n\n${parseHumanReadableError(parseResult.error.issues)}`,
       fallbackOutput,
diff --git a/packages/app/src/cli/models/extensions/specifications/validation/app_config_webhook.ts b/packages/app/src/cli/models/extensions/specifications/validation/app_config_webhook.ts
index e379ca2ccd..247274ead7 100644
--- a/packages/app/src/cli/models/extensions/specifications/validation/app_config_webhook.ts
+++ b/packages/app/src/cli/models/extensions/specifications/validation/app_config_webhook.ts
@@ -1,5 +1,6 @@
 import {zod} from '@shopify/cli-kit/node/schema'
 import {uniq} from '@shopify/cli-kit/common/array'
+import colors from '@shopify/cli-kit/node/colors'
 import type {WebhooksConfig} from '../types/app_config_webhook.js'
 
 export function webhookValidator(schema: object, ctx: zod.RefinementCtx) {
@@ -14,6 +15,7 @@ export function webhookValidator(schema: object, ctx: zod.RefinementCtx) {
 function validateSubscriptions(webhookConfig: WebhooksConfig) {
   const {subscriptions = []} = webhookConfig
   const uniqueSubscriptionSet = new Set()
+  const duplicatedSubscriptionsFields: string[] = []
 
   if (!subscriptions.length) return
 
@@ -49,19 +51,28 @@ function validateSubscriptions(webhookConfig: WebhooksConfig) {
       }
     }
 
-    for (const [j, topic] of topics.entries()) {
+    topics.forEach((topic) => {
       const key = `${topic}::${uri}::${filter}`
 
       if (uniqueSubscriptionSet.has(key)) {
-        return {
-          code: zod.ZodIssueCode.custom,
-          message: 'You can’t have duplicate subscriptions with the exact same `topic`, `uri` and `filter`',
-          fatal: true,
-          path: [...path, 'topics', j, topic],
-        }
+        const subscriptionFieldsString = filter
+          ? colors.dim(`\n\ntopic: ${topic}\nuri: ${uri}\nfilter: ${filter}`)
+          : colors.dim(`\n\ntopic: ${topic}\nuri: ${uri}`)
+
+        duplicatedSubscriptionsFields.push(subscriptionFieldsString)
       }
 
       uniqueSubscriptionSet.add(key)
+    })
+  }
+
+  if (duplicatedSubscriptionsFields.length > 0) {
+    const fieldsArrToString = duplicatedSubscriptionsFields.join('')
+
+    return {
+      code: zod.ZodIssueCode.custom,
+      message: `Multiple subscriptions with the exact same topic, uri, and filter. To resolve, remove or edit the duplicates ${fieldsArrToString}`,
+      path: ['subscriptions'],
     }
   }
 }