diff --git a/bin/get-graphql-schemas.js b/bin/get-graphql-schemas.js
index 886ec935094..31685438520 100755
--- a/bin/get-graphql-schemas.js
+++ b/bin/get-graphql-schemas.js
@@ -38,6 +38,12 @@ const schemas = [
     repo: 'shopify',
     pathToFile: 'areas/core/shopify/db/graphql/admin_schema_unstable_public.graphql',
     localPath: './packages/cli-kit/src/cli/api/graphql/admin/admin_schema.graphql',
+  },
+  {
+    repo: 'shopify',
+    pathToFile: 'areas/core/shopify/db/graphql/webhooks_schema_unstable_public.graphql',
+    localPath: './packages/app/src/cli/api/graphql/webhooks/webhooks_schema.graphql',
+    branch: 'dd',
   }
 ]
 
diff --git a/graphql.config.ts b/graphql.config.ts
index b1a5c631f2d..e101f3635d2 100644
--- a/graphql.config.ts
+++ b/graphql.config.ts
@@ -1,7 +1,10 @@
 function projectFactory(name: string, schemaName: string, project: string = 'app') {
   return {
     schema: `./packages/${project}/src/cli/api/graphql/${name}/${schemaName}`,
-    documents: [`./packages/${project}/src/cli/api/graphql/${name}/queries/**/*.graphql`,`./packages/${project}/src/cli/api/graphql/${name}/mutations/**/*.graphql`],
+    documents: [
+      `./packages/${project}/src/cli/api/graphql/${name}/queries/**/*.graphql`,
+      `./packages/${project}/src/cli/api/graphql/${name}/mutations/**/*.graphql`,
+    ],
     extensions: {
       codegen: {
         generates: {
@@ -78,5 +81,6 @@ export default {
     appDev: projectFactory('app-dev', 'app_dev_schema.graphql'),
     appManagement: projectFactory('app-management', 'app_management_schema.graphql'),
     admin: projectFactory('admin', 'admin_schema.graphql', 'cli-kit'),
+    webhooks: projectFactory('webhooks', 'webhooks_schema.graphql'),
   },
 }
diff --git a/nx.json b/nx.json
index c824586b865..ec761c37fc1 100644
--- a/nx.json
+++ b/nx.json
@@ -54,6 +54,7 @@
           "build:types",
           "graphql-codegen:generate:business-platform",
           "graphql-codegen:generate:partners",
+          "graphql-codegen:generate:webhooks",
           "graphql-codegen:postfix",
           "graphql-codegen:formatting"
         ],
diff --git a/packages/app/project.json b/packages/app/project.json
index 9bf718c9f18..696d41e380a 100644
--- a/packages/app/project.json
+++ b/packages/app/project.json
@@ -80,7 +80,8 @@
         "{projectRoot}/src/cli/api/graphql/business-platform-destinations/generated/**/*.ts",
         "{projectRoot}/src/cli/api/graphql/business-platform-organizations/generated/**/*.ts",
         "{projectRoot}/src/cli/api/graphql/app-dev/generated/**/*.ts",
-        "{projectRoot}/src/cli/api/graphql/app-management/generated/**/*.ts"
+        "{projectRoot}/src/cli/api/graphql/app-management/generated/**/*.ts",
+        "{projectRoot}/src/cli/api/graphql/webhooks/generated/**/*.ts"
       ],
       "options": {
         "commands": [
@@ -88,7 +89,8 @@
           "pnpm eslint 'src/cli/api/graphql/business-platform-destinations/generated/**/*.{ts,tsx}' --fix",
           "pnpm eslint 'src/cli/api/graphql/business-platform-organizations/generated/**/*.{ts,tsx}' --fix",
           "pnpm eslint 'src/cli/api/graphql/app-dev/generated/**/*.{ts,tsx}' --fix",
-          "pnpm eslint 'src/cli/api/graphql/app-management/generated/**/*.{ts,tsx}' --fix"
+          "pnpm eslint 'src/cli/api/graphql/app-management/generated/**/*.{ts,tsx}' --fix",
+          "pnpm eslint 'src/cli/api/graphql/webhooks/generated/**/*.{ts,tsx}' --fix"
         ],
         "cwd": "packages/app"
       }
@@ -137,6 +139,17 @@
         "cwd": "{workspaceRoot}"
       }
     },
+    "graphql-codegen:generate:webhooks": {
+      "executor": "nx:run-commands",
+      "inputs": ["{workspaceRoot}/graphql.config.ts", "{projectRoot}/src/cli/api/graphql/webhooks/**/*.graphql"],
+      "outputs": ["{projectRoot}/src/cli/api/graphql/webhooks/generated/**/*.ts"],
+      "options": {
+        "commands": [
+          "pnpm exec graphql-codegen --project=webhooks"
+        ],
+        "cwd": "{workspaceRoot}"
+      }
+    },
     "graphql-codegen:generate:app-management": {
       "executor": "nx:run-commands",
       "inputs": ["{workspaceRoot}/graphql.config.ts", "{projectRoot}/src/cli/api/graphql/app-management/**/*.graphql"],
@@ -155,7 +168,8 @@
         "graphql-codegen:generate:business-platform-destinations",
         "graphql-codegen:generate:business-platform-organizations",
         "graphql-codegen:generate:app-dev",
-        "graphql-codegen:generate:app-management"
+        "graphql-codegen:generate:app-management",
+        "graphql-codegen:generate:webhooks"
       ],
       "inputs": [{ "dependentTasksOutputFiles": "**/*.ts" }],
       "outputs": [
@@ -163,7 +177,8 @@
         "{projectRoot}/src/cli/api/graphql/business-platform-destinations/generated/**/*.ts",
         "{projectRoot}/src/cli/api/graphql/business-platform-organizations/generated/**/*.ts",
         "{projectRoot}/src/cli/api/graphql/app-dev/generated/**/*.ts",
-        "{projectRoot}/src/cli/api/graphql/app-management/generated/**/*.ts"
+        "{projectRoot}/src/cli/api/graphql/app-management/generated/**/*.ts",
+        "{projectRoot}/src/cli/api/graphql/webhooks/generated/**/*.ts"
       ],
       "options": {
         "commands": [
@@ -171,7 +186,8 @@
           "find ./packages/app/src/cli/api/graphql/business-platform-destinations/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;",
           "find ./packages/app/src/cli/api/graphql/business-platform-organizations/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;",
           "find ./packages/app/src/cli/api/graphql/app-dev/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;",
-          "find ./packages/app/src/cli/api/graphql/app-management/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;"
+          "find ./packages/app/src/cli/api/graphql/app-management/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;",
+          "find ./packages/app/src/cli/api/graphql/webhooks/generated/ -type f -name '*.ts' -exec sh -c 'sed -i \"\" \"s|import \\* as Types from '\\''./types'\\'';|import \\* as Types from '\\''./types.js'\\'';|g; s|export const \\([A-Za-z0-9_]*\\)Document =|export const \\1 =|g\" \"$0\"' {} \\;"
         ],
         "cwd": "{workspaceRoot}"
       }
diff --git a/packages/app/src/cli/api/graphql/webhooks/generated/available-topics.ts b/packages/app/src/cli/api/graphql/webhooks/generated/available-topics.ts
new file mode 100644
index 00000000000..5d800b5bdf6
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/generated/available-topics.ts
@@ -0,0 +1,44 @@
+/* eslint-disable @typescript-eslint/consistent-type-definitions */
+import * as Types from './types.js'
+
+import {TypedDocumentNode as DocumentNode} from '@graphql-typed-document-node/core'
+
+export type AvailableTopicsQueryVariables = Types.Exact<{
+  apiVersion: Types.Scalars['String']['input']
+}>
+
+export type AvailableTopicsQuery = {availableTopics?: string[] | null}
+
+export const AvailableTopics = {
+  kind: 'Document',
+  definitions: [
+    {
+      kind: 'OperationDefinition',
+      operation: 'query',
+      name: {kind: 'Name', value: 'availableTopics'},
+      variableDefinitions: [
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'apiVersion'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+      ],
+      selectionSet: {
+        kind: 'SelectionSet',
+        selections: [
+          {
+            kind: 'Field',
+            name: {kind: 'Name', value: 'availableTopics'},
+            arguments: [
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'apiVersion'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'apiVersion'}},
+              },
+            ],
+          },
+        ],
+      },
+    },
+  ],
+} as unknown as DocumentNode<AvailableTopicsQuery, AvailableTopicsQueryVariables>
diff --git a/packages/app/src/cli/api/graphql/webhooks/generated/cli-testing.ts b/packages/app/src/cli/api/graphql/webhooks/generated/cli-testing.ts
new file mode 100644
index 00000000000..a15253d2cc6
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/generated/cli-testing.ts
@@ -0,0 +1,111 @@
+/* eslint-disable @typescript-eslint/consistent-type-definitions */
+import * as Types from './types.js'
+
+import {TypedDocumentNode as DocumentNode} from '@graphql-typed-document-node/core'
+
+export type CliTestingMutationVariables = Types.Exact<{
+  address: Types.Scalars['String']['input']
+  apiKey?: Types.InputMaybe<Types.Scalars['String']['input']>
+  apiVersion: Types.Scalars['String']['input']
+  deliveryMethod: Types.Scalars['String']['input']
+  sharedSecret: Types.Scalars['String']['input']
+  topic: Types.Scalars['String']['input']
+}>
+
+export type CliTestingMutation = {
+  cliTesting?: {headers?: string | null; samplePayload?: string | null; success: boolean; errors: string[]} | null
+}
+
+export const CliTesting = {
+  kind: 'Document',
+  definitions: [
+    {
+      kind: 'OperationDefinition',
+      operation: 'mutation',
+      name: {kind: 'Name', value: 'CliTesting'},
+      variableDefinitions: [
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'address'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'apiKey'}},
+          type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}},
+        },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'apiVersion'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'deliveryMethod'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'sharedSecret'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+        {
+          kind: 'VariableDefinition',
+          variable: {kind: 'Variable', name: {kind: 'Name', value: 'topic'}},
+          type: {kind: 'NonNullType', type: {kind: 'NamedType', name: {kind: 'Name', value: 'String'}}},
+        },
+      ],
+      selectionSet: {
+        kind: 'SelectionSet',
+        selections: [
+          {
+            kind: 'Field',
+            name: {kind: 'Name', value: 'cliTesting'},
+            arguments: [
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'address'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'address'}},
+              },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'apiKey'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'apiKey'}},
+              },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'apiVersion'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'apiVersion'}},
+              },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'deliveryMethod'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'deliveryMethod'}},
+              },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'sharedSecret'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'sharedSecret'}},
+              },
+              {
+                kind: 'Argument',
+                name: {kind: 'Name', value: 'topic'},
+                value: {kind: 'Variable', name: {kind: 'Name', value: 'topic'}},
+              },
+            ],
+            selectionSet: {
+              kind: 'SelectionSet',
+              selections: [
+                {kind: 'Field', name: {kind: 'Name', value: 'headers'}},
+                {kind: 'Field', name: {kind: 'Name', value: 'samplePayload'}},
+                {kind: 'Field', name: {kind: 'Name', value: 'success'}},
+                {kind: 'Field', name: {kind: 'Name', value: 'errors'}},
+                {kind: 'Field', name: {kind: 'Name', value: '__typename'}},
+              ],
+            },
+          },
+        ],
+      },
+    },
+  ],
+} as unknown as DocumentNode<CliTestingMutation, CliTestingMutationVariables>
diff --git a/packages/app/src/cli/api/graphql/webhooks/generated/public-api-versions.ts b/packages/app/src/cli/api/graphql/webhooks/generated/public-api-versions.ts
new file mode 100644
index 00000000000..c5cc702cd1f
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/generated/public-api-versions.ts
@@ -0,0 +1,35 @@
+/* eslint-disable @typescript-eslint/consistent-type-definitions */
+import * as Types from './types.js'
+
+import {TypedDocumentNode as DocumentNode} from '@graphql-typed-document-node/core'
+
+export type PublicApiVersionsQueryVariables = Types.Exact<{[key: string]: never}>
+
+export type PublicApiVersionsQuery = {publicApiVersions: {handle: string}[]}
+
+export const PublicApiVersions = {
+  kind: 'Document',
+  definitions: [
+    {
+      kind: 'OperationDefinition',
+      operation: 'query',
+      name: {kind: 'Name', value: 'publicApiVersions'},
+      selectionSet: {
+        kind: 'SelectionSet',
+        selections: [
+          {
+            kind: 'Field',
+            name: {kind: 'Name', value: 'publicApiVersions'},
+            selectionSet: {
+              kind: 'SelectionSet',
+              selections: [
+                {kind: 'Field', name: {kind: 'Name', value: 'handle'}},
+                {kind: 'Field', name: {kind: 'Name', value: '__typename'}},
+              ],
+            },
+          },
+        ],
+      },
+    },
+  ],
+} as unknown as DocumentNode<PublicApiVersionsQuery, PublicApiVersionsQueryVariables>
diff --git a/packages/app/src/cli/api/graphql/webhooks/generated/types.d.ts b/packages/app/src/cli/api/graphql/webhooks/generated/types.d.ts
new file mode 100644
index 00000000000..2b9d2b25a6f
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/generated/types.d.ts
@@ -0,0 +1,16 @@
+/* eslint-disable @typescript-eslint/consistent-type-definitions, @typescript-eslint/naming-convention  */
+export type Maybe<T> = T | null
+export type InputMaybe<T> = Maybe<T>
+export type Exact<T extends {[key: string]: unknown}> = {[K in keyof T]: T[K]}
+export type MakeOptional<T, K extends keyof T> = Omit<T, K> & {[SubKey in K]?: Maybe<T[SubKey]>}
+export type MakeMaybe<T, K extends keyof T> = Omit<T, K> & {[SubKey in K]: Maybe<T[SubKey]>}
+export type MakeEmpty<T extends {[key: string]: unknown}, K extends keyof T> = {[_ in K]?: never}
+export type Incremental<T> = T | {[P in keyof T]?: P extends ' $fragmentName' | '__typename' ? T[P] : never}
+/** All built-in and custom scalars, mapped to their actual values */
+export type Scalars = {
+  ID: {input: string; output: string}
+  String: {input: string; output: string}
+  Boolean: {input: boolean; output: boolean}
+  Int: {input: number; output: number}
+  Float: {input: number; output: number}
+}
diff --git a/packages/app/src/cli/api/graphql/webhooks/queries/available-topics.graphql b/packages/app/src/cli/api/graphql/webhooks/queries/available-topics.graphql
new file mode 100644
index 00000000000..5fea722e663
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/queries/available-topics.graphql
@@ -0,0 +1,3 @@
+query availableTopics($apiVersion: String!) {
+  availableTopics(apiVersion: $apiVersion)
+}
diff --git a/packages/app/src/cli/api/graphql/webhooks/queries/cli-testing.graphql b/packages/app/src/cli/api/graphql/webhooks/queries/cli-testing.graphql
new file mode 100644
index 00000000000..06b29c75bd8
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/queries/cli-testing.graphql
@@ -0,0 +1,8 @@
+mutation CliTesting($address: String!, $apiKey: String, $apiVersion: String!, $deliveryMethod: String!, $sharedSecret: String!, $topic: String!) {
+  cliTesting(address: $address, apiKey: $apiKey, apiVersion: $apiVersion, deliveryMethod: $deliveryMethod, sharedSecret: $sharedSecret, topic: $topic) {
+    headers
+    samplePayload
+    success
+    errors
+  }
+}
diff --git a/packages/app/src/cli/api/graphql/webhooks/queries/public-api-versions.graphql b/packages/app/src/cli/api/graphql/webhooks/queries/public-api-versions.graphql
new file mode 100644
index 00000000000..03da5ff5ff4
--- /dev/null
+++ b/packages/app/src/cli/api/graphql/webhooks/queries/public-api-versions.graphql
@@ -0,0 +1,5 @@
+query publicApiVersions {
+  publicApiVersions {
+    handle
+  }
+}
diff --git a/packages/app/src/cli/commands/app/webhook/trigger.ts b/packages/app/src/cli/commands/app/webhook/trigger.ts
index d6500fd8e22..2bf6e865998 100644
--- a/packages/app/src/cli/commands/app/webhook/trigger.ts
+++ b/packages/app/src/cli/commands/app/webhook/trigger.ts
@@ -115,6 +115,7 @@ export default class WebhookTrigger extends AppCommand {
       clientSecret: flags['client-secret'] || flags['shared-secret'],
       path: flags.path,
       config: flags.config,
+      organizationId: appContextResult.organization.id,
     }
 
     await webhookTriggerService(usedFlags)
diff --git a/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts b/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
index 27c528eef38..46df212335b 100644
--- a/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
+++ b/packages/app/src/cli/services/dev/processes/setup-dev-processes.ts
@@ -156,6 +156,7 @@ export async function setupDevProcesses({
       webs: reloadedApp.webs,
       backendPort: network.backendPort,
       frontendPort: network.frontendPort,
+      organizationId: remoteApp.organizationId,
       developerPlatformClient,
       storeFqdn,
       apiSecret,
diff --git a/packages/app/src/cli/services/dev/processes/uninstall-webhook.ts b/packages/app/src/cli/services/dev/processes/uninstall-webhook.ts
index f7d4cad2681..af73a463a70 100644
--- a/packages/app/src/cli/services/dev/processes/uninstall-webhook.ts
+++ b/packages/app/src/cli/services/dev/processes/uninstall-webhook.ts
@@ -10,6 +10,7 @@ interface SendWebhookOptions {
   storeFqdn: string
   apiSecret: string
   webhooksPath: string
+  organizationId: string
 }
 
 export interface SendWebhookProcess extends BaseProcess<SendWebhookOptions> {
@@ -23,6 +24,7 @@ export const sendWebhook: DevProcessFunction<SendWebhookOptions> = async ({stdou
     address: `http://localhost:${options.deliveryPort}${options.webhooksPath}`,
     sharedSecret: options.apiSecret,
     storeFqdn: options.storeFqdn,
+    organizationId: options.organizationId,
   })
 }
 
@@ -31,12 +33,14 @@ export function setupSendUninstallWebhookProcess({
   remoteAppUpdated,
   backendPort,
   frontendPort,
+  organizationId,
   ...options
 }: Pick<SendWebhookOptions, 'developerPlatformClient' | 'storeFqdn' | 'apiSecret'> & {
   remoteAppUpdated: boolean
   backendPort: number
   frontendPort: number
   webs: Web[]
+  organizationId: string
 }): SendWebhookProcess | undefined {
   const {backendConfig, frontendConfig} = frontAndBackendConfig(webs)
   const webhooksPath =
@@ -52,6 +56,7 @@ export function setupSendUninstallWebhookProcess({
     options: {
       deliveryPort: backendConfig ? backendPort : frontendPort,
       webhooksPath,
+      organizationId,
       ...options,
     },
   }
diff --git a/packages/app/src/cli/services/webhook/request-api-versions.test.ts b/packages/app/src/cli/services/webhook/request-api-versions.test.ts
index 3d071fa90ed..4f3777fc4d4 100644
--- a/packages/app/src/cli/services/webhook/request-api-versions.test.ts
+++ b/packages/app/src/cli/services/webhook/request-api-versions.test.ts
@@ -5,7 +5,8 @@ import {describe, expect, test} from 'vitest'
 describe('requestApiVersions', () => {
   test('calls partners to request data and returns ordered array', async () => {
     // Given - When
-    const got = await requestApiVersions(testDeveloperPlatformClient())
+    const organizationId = 'organizationId'
+    const got = await requestApiVersions(testDeveloperPlatformClient(), organizationId)
 
     // Then
     expect(got).toEqual(['2023', '2022', 'unstable'])
diff --git a/packages/app/src/cli/services/webhook/request-api-versions.ts b/packages/app/src/cli/services/webhook/request-api-versions.ts
index 2e94a9a510e..0a0d1eb9304 100644
--- a/packages/app/src/cli/services/webhook/request-api-versions.ts
+++ b/packages/app/src/cli/services/webhook/request-api-versions.ts
@@ -14,10 +14,14 @@ export const GetApiVersionsQuery = `
  * Requests available api-versions in order to validate flags or present a list of options
  *
  * @param developerPlatformClient - The client to access the platform API
+ * @param organizationId - Organization ID required by the API to verify permissions
  * @returns List of public api-versions
  */
-export async function requestApiVersions(developerPlatformClient: DeveloperPlatformClient): Promise<string[]> {
-  const {publicApiVersions: result}: PublicApiVersionsSchema = await developerPlatformClient.apiVersions()
+export async function requestApiVersions(
+  developerPlatformClient: DeveloperPlatformClient,
+  organizationId: string,
+): Promise<string[]> {
+  const {publicApiVersions: result}: PublicApiVersionsSchema = await developerPlatformClient.apiVersions(organizationId)
 
   const unstableIdx = result.indexOf('unstable')
   if (unstableIdx === -1) {
diff --git a/packages/app/src/cli/services/webhook/request-sample.test.ts b/packages/app/src/cli/services/webhook/request-sample.test.ts
index 943cafead03..0a675556e34 100644
--- a/packages/app/src/cli/services/webhook/request-sample.test.ts
+++ b/packages/app/src/cli/services/webhook/request-sample.test.ts
@@ -9,10 +9,12 @@ const inputValues: SendSampleWebhookVariables = {
   address: 'https://example.org',
   shared_secret: 'A_SECRET',
 }
+const organizationId = 'organizationId'
+
 describe('getWebhookSample', () => {
   test('calls partners to request data without api-key', async () => {
     // Given/When
-    const got = await getWebhookSample(testDeveloperPlatformClient(), inputValues)
+    const got = await getWebhookSample(testDeveloperPlatformClient(), inputValues, organizationId)
 
     // Then
     expect(got.samplePayload).toEqual('{ "sampleField": "SampleValue" }')
@@ -29,7 +31,7 @@ describe('getWebhookSample', () => {
     }
 
     // When
-    const got = await getWebhookSample(testDeveloperPlatformClient(), variables)
+    const got = await getWebhookSample(testDeveloperPlatformClient(), variables, organizationId)
 
     // Then
     expect(got.samplePayload).toEqual('{ "sampleField": "SampleValue" }')
diff --git a/packages/app/src/cli/services/webhook/request-sample.ts b/packages/app/src/cli/services/webhook/request-sample.ts
index 68d88edeec4..b6c6ab813c5 100644
--- a/packages/app/src/cli/services/webhook/request-sample.ts
+++ b/packages/app/src/cli/services/webhook/request-sample.ts
@@ -25,6 +25,7 @@ export interface UserErrors {
   fields: string[]
 }
 
+// eslint-disable-next-line @shopify/cli/no-inline-graphql
 export const sendSampleWebhookMutation = `
   mutation samplePayload($topic: String!, $api_version: String!, $address: String!, $delivery_method: String!, $shared_secret: String!, $api_key: String) {
     sendSampleWebhook(input: {topic: $topic, apiVersion: $api_version, address: $address, deliveryMethod: $delivery_method, sharedSecret: $shared_secret, apiKey: $api_key}) {
@@ -53,14 +54,17 @@ export const sendSampleWebhookMutation = `
  *  - address - A destination for the webhook notification
  *  - shared_secret - A secret to generate the HMAC header apps can use to validate the origin
  *  - api_key - Client Api Key required to validate Event-Bridge addresses (optional)
+ * @param organizationId - Organization ID required by the API to verify permissions
  * @returns Empty if a remote delivery was requested, payload data if a local delivery was requested
  */
 export async function getWebhookSample(
   developerPlatformClient: DeveloperPlatformClient,
   variables: SendSampleWebhookVariables,
+  organizationId: string,
 ): Promise<SampleWebhook> {
   const {sendSampleWebhook: result}: SendSampleWebhookSchema = await developerPlatformClient.sendSampleWebhook(
     variables,
+    organizationId,
   )
 
   return result
diff --git a/packages/app/src/cli/services/webhook/request-topics.test.ts b/packages/app/src/cli/services/webhook/request-topics.test.ts
index e0267d856fa..83a680fd428 100644
--- a/packages/app/src/cli/services/webhook/request-topics.test.ts
+++ b/packages/app/src/cli/services/webhook/request-topics.test.ts
@@ -3,11 +3,12 @@ import {testDeveloperPlatformClient} from '../../models/app/app.test-data.js'
 import {describe, expect, test} from 'vitest'
 
 const aVersion = 'SOME_VERSION'
+const anOrganizationId = 'organizationId'
 
 describe('requestTopics', () => {
   test('calls partners to request topics data and returns array', async () => {
     // Given/When
-    const got = await requestTopics(testDeveloperPlatformClient(), aVersion)
+    const got = await requestTopics(testDeveloperPlatformClient(), aVersion, anOrganizationId)
 
     // Then
     expect(got).toEqual(['orders/create', 'shop/redact'])
diff --git a/packages/app/src/cli/services/webhook/request-topics.ts b/packages/app/src/cli/services/webhook/request-topics.ts
index f8b3bdc9f2d..f93a162e3a7 100644
--- a/packages/app/src/cli/services/webhook/request-topics.ts
+++ b/packages/app/src/cli/services/webhook/request-topics.ts
@@ -19,14 +19,16 @@ export const getTopicsQuery = `
  *
  * @param developerPlatformClient - The client to access the platform API
  * @param apiVersion - ApiVersion of the topics
+ * @param organizationId - Organization ID required by the API to verify permissions
  * @returns - Available webhook topics for the api-version
  */
 export async function requestTopics(
   developerPlatformClient: DeveloperPlatformClient,
   apiVersion: string,
+  organizationId: string,
 ): Promise<string[]> {
   const variables: WebhookTopicsVariables = {api_version: apiVersion}
-  const {webhookTopics: result}: WebhookTopicsSchema = await developerPlatformClient.topics(variables)
+  const {webhookTopics: result}: WebhookTopicsSchema = await developerPlatformClient.topics(variables, organizationId)
 
   return result
 }
diff --git a/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.test.ts b/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.test.ts
index da1d3d3b6c5..025c8ac52dd 100644
--- a/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.test.ts
+++ b/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.test.ts
@@ -10,6 +10,7 @@ vi.mock('@shopify/cli-kit/node/system')
 
 const address = 'http://localhost:3000/test/path'
 const storeFqdn = 'test-store.myshopify.io'
+const organizationId = 'organizationId'
 
 describe('sendUninstallWebhookToAppServer', () => {
   test('requests sample and API versions, triggers local webhook', async () => {
@@ -22,6 +23,7 @@ describe('sendUninstallWebhookToAppServer', () => {
       sharedSecret: 'sharedSecret',
       storeFqdn,
       developerPlatformClient: testDeveloperPlatformClient(),
+      organizationId,
     })
 
     expect(result).toBe(true)
@@ -45,6 +47,7 @@ describe('sendUninstallWebhookToAppServer', () => {
       sharedSecret: 'sharedSecret',
       storeFqdn,
       developerPlatformClient,
+      organizationId,
     })
 
     expect(result).toBe(false)
@@ -68,6 +71,7 @@ describe('sendUninstallWebhookToAppServer', () => {
       sharedSecret: 'sharedSecret',
       storeFqdn,
       developerPlatformClient,
+      organizationId,
     })
 
     expect(result).toBe(true)
diff --git a/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.ts b/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.ts
index 38cdc1fc0a7..a8581936c01 100644
--- a/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.ts
+++ b/packages/app/src/cli/services/webhook/send-app-uninstalled-webhook.ts
@@ -13,12 +13,13 @@ interface SendUninstallWebhookToAppServerOptions {
   storeFqdn: string
   address: string
   sharedSecret: string
+  organizationId: string
 }
 
 export async function sendUninstallWebhookToAppServer(
   options: SendUninstallWebhookToAppServerOptions,
 ): Promise<boolean> {
-  const apiVersions = await requestApiVersions(options.developerPlatformClient)
+  const apiVersions = await requestApiVersions(options.developerPlatformClient, options.organizationId)
   const variables: SendSampleWebhookVariables = {
     topic: 'app/uninstalled',
     // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
@@ -27,7 +28,7 @@ export async function sendUninstallWebhookToAppServer(
     delivery_method: DELIVERY_METHOD.LOCALHOST,
     shared_secret: options.sharedSecret,
   }
-  const sample = await getWebhookSample(options.developerPlatformClient, variables)
+  const sample = await getWebhookSample(options.developerPlatformClient, variables, options.organizationId)
 
   options.stdout.write('Sending APP_UNINSTALLED webhook to app server')
 
diff --git a/packages/app/src/cli/services/webhook/trigger-options.test.ts b/packages/app/src/cli/services/webhook/trigger-options.test.ts
index 3dcc2c25dcb..ab8a5afb562 100644
--- a/packages/app/src/cli/services/webhook/trigger-options.test.ts
+++ b/packages/app/src/cli/services/webhook/trigger-options.test.ts
@@ -18,6 +18,7 @@ const API_KEY = 'AN_API_KEY'
 const APP = testAppLinked()
 const ORGANIZATION_APP = testOrganizationApp()
 const developerPlatformClient = testDeveloperPlatformClient()
+const organizationId = ORGANIZATION_APP.organizationId
 
 afterEach(() => {
   mockAndCaptureOutput().clear()
@@ -30,7 +31,7 @@ describe('collectApiVersion', () => {
     vi.mocked(apiVersionPrompt)
 
     // When
-    const version = await collectApiVersion(developerPlatformClient, '2023-01')
+    const version = await collectApiVersion(developerPlatformClient, '2023-01', organizationId)
 
     // Then
     expect(version).toEqual('2023-01')
@@ -43,7 +44,7 @@ describe('collectApiVersion', () => {
     vi.mocked(requestApiVersions).mockResolvedValue(['2023-01', 'unstable'])
 
     // When
-    const version = await collectApiVersion(developerPlatformClient, undefined)
+    const version = await collectApiVersion(developerPlatformClient, undefined, organizationId)
 
     // Then
     expect(version).toEqual('2023-01')
@@ -59,7 +60,12 @@ describe('collectTopic', () => {
     vi.mocked(requestTopics).mockResolvedValue(['shop/redact', 'orders/create'])
 
     // When
-    const method = await collectTopic(developerPlatformClient, '2023-01', 'shop/redact')
+    const method = await collectTopic(
+      developerPlatformClient,
+      '2023-01',
+      'shop/redact',
+      ORGANIZATION_APP.organizationId,
+    )
 
     // Then
     expect(method).toEqual('shop/redact')
@@ -72,7 +78,9 @@ describe('collectTopic', () => {
     vi.mocked(requestTopics).mockResolvedValue(['shop/redact', 'orders/create'])
 
     // When then
-    await expect(collectTopic(developerPlatformClient, '2023-01', 'unknown/topic')).rejects.toThrow(AbortError)
+    await expect(collectTopic(developerPlatformClient, '2023-01', 'unknown/topic', organizationId)).rejects.toThrow(
+      AbortError,
+    )
     expect(topicPrompt).toHaveBeenCalledTimes(0)
   })
 
@@ -82,7 +90,7 @@ describe('collectTopic', () => {
     vi.mocked(requestTopics).mockResolvedValue(['shop/redact', 'orders/create'])
 
     // When
-    const topic = await collectTopic(developerPlatformClient, 'unstable', undefined)
+    const topic = await collectTopic(developerPlatformClient, 'unstable', undefined, organizationId)
 
     // Then
     expect(topic).toEqual('orders/create')
diff --git a/packages/app/src/cli/services/webhook/trigger-options.ts b/packages/app/src/cli/services/webhook/trigger-options.ts
index b7181bf98dc..26ca2da3838 100644
--- a/packages/app/src/cli/services/webhook/trigger-options.ts
+++ b/packages/app/src/cli/services/webhook/trigger-options.ts
@@ -59,13 +59,15 @@ export async function collectCredentials(
  *
  * @param developerPlatformClient - The client to access the platform API
  * @param apiVersion - VALID or undefined api-version
+ * @param organizationId - Organization ID required by the API to verify permissions
  * @returns api-version
  */
 export async function collectApiVersion(
   developerPlatformClient: DeveloperPlatformClient,
   apiVersion: string | undefined,
+  organizationId: string,
 ): Promise<string> {
-  const apiVersions = await requestApiVersions(developerPlatformClient)
+  const apiVersions = await requestApiVersions(developerPlatformClient, organizationId)
   if (apiVersion) return parseApiVersionFlag(apiVersion, apiVersions)
   return apiVersionPrompt(apiVersions)
 }
@@ -76,18 +78,19 @@ export async function collectApiVersion(
  * @param developerPlatformClient - The client to access the platform API
  * @param apiVersion - VALID api-version
  * @param topic - topic or undefined
+ * @param organizationId - Organization ID required by the API to verify permissions
  * @returns topic
  */
 export async function collectTopic(
   developerPlatformClient: DeveloperPlatformClient,
   apiVersion: string,
   topic: string | undefined,
+  organizationId: string,
 ): Promise<string> {
+  const topics = await requestTopics(developerPlatformClient, apiVersion, organizationId)
   if (topic) {
-    return parseTopicFlag(topic, apiVersion, await requestTopics(developerPlatformClient, apiVersion))
+    return parseTopicFlag(topic, apiVersion, topics)
   }
-
-  const topics = await requestTopics(developerPlatformClient, apiVersion)
   return topicPrompt(topics)
 }
 
diff --git a/packages/app/src/cli/services/webhook/trigger.test.ts b/packages/app/src/cli/services/webhook/trigger.test.ts
index 26541d4559d..b17e1d22be1 100644
--- a/packages/app/src/cli/services/webhook/trigger.test.ts
+++ b/packages/app/src/cli/services/webhook/trigger.test.ts
@@ -23,6 +23,7 @@ const aPort = '1234'
 const aUrlPath = '/a/url/path'
 const anAddress = 'https://example.org'
 const anEventBridgeAddress = 'arn:aws:events:us-east-3::event-source/aws.partner/shopify.com/12/source'
+const anOrganizationId = 'anOrganizationId'
 
 vi.mock('@shopify/cli-kit')
 vi.mock('@shopify/cli-kit/node/output')
@@ -81,7 +82,7 @@ describe('webhookTriggerService', () => {
     await webhookTriggerService(sampleFlags())
 
     // Then
-    expectCalls(aVersion)
+    expectCalls(aVersion, anOrganizationId)
     expect(consoleError).toHaveBeenCalledWith(`Request errors:\n  · Some error\n  · Another error`)
   })
 
@@ -104,7 +105,7 @@ describe('webhookTriggerService', () => {
     await webhookTriggerService(sampleFlags())
 
     // Then
-    expectCalls(aVersion)
+    expectCalls(aVersion, anOrganizationId)
     expect(consoleError).toHaveBeenCalledWith(`Request errors:\n${JSON.stringify(response.userErrors)}`)
   })
 
@@ -125,8 +126,12 @@ describe('webhookTriggerService', () => {
     await webhookTriggerService(sampleFlags())
 
     // Then
-    expectCalls(aVersion)
-    expect(getWebhookSample).toHaveBeenCalledWith(developerPlatformClient, expectedSampleWebhookVariables)
+    expectCalls(aVersion, anOrganizationId)
+    expect(getWebhookSample).toHaveBeenCalledWith(
+      developerPlatformClient,
+      expectedSampleWebhookVariables,
+      anOrganizationId,
+    )
     expect(triggerLocalWebhook).toHaveBeenCalledTimes(0)
     expect(outputSuccess).toHaveBeenCalledWith('Webhook has been enqueued for delivery')
   })
@@ -174,8 +179,12 @@ describe('webhookTriggerService', () => {
     await webhookTriggerService(flags)
 
     // Then
-    expectCalls(aVersion)
-    expect(getWebhookSample).toHaveBeenCalledWith(developerPlatformClient, expectedSampleWebhookVariables)
+    expectCalls(aVersion, anOrganizationId)
+    expect(getWebhookSample).toHaveBeenCalledWith(
+      developerPlatformClient,
+      expectedSampleWebhookVariables,
+      anOrganizationId,
+    )
     expect(outputSuccess).toHaveBeenCalledWith('Webhook has been enqueued for delivery')
   })
 
@@ -197,8 +206,12 @@ describe('webhookTriggerService', () => {
       await webhookTriggerService(sampleLocalhostFlags())
 
       // Then
-      expectCalls(aVersion)
-      expect(getWebhookSample).toHaveBeenCalledWith(developerPlatformClient, expectedSampleWebhookVariables)
+      expectCalls(aVersion, anOrganizationId)
+      expect(getWebhookSample).toHaveBeenCalledWith(
+        developerPlatformClient,
+        expectedSampleWebhookVariables,
+        anOrganizationId,
+      )
       expect(triggerLocalWebhook).toHaveBeenCalledWith(aFullLocalAddress, samplePayload, sampleHeaders)
       expect(outputSuccess).toHaveBeenCalledWith('Localhost delivery sucessful')
     })
@@ -220,8 +233,12 @@ describe('webhookTriggerService', () => {
       await webhookTriggerService(sampleLocalhostFlags())
 
       // Then
-      expectCalls(aVersion)
-      expect(getWebhookSample).toHaveBeenCalledWith(developerPlatformClient, expectedSampleWebhookVariables)
+      expectCalls(aVersion, anOrganizationId)
+      expect(getWebhookSample).toHaveBeenCalledWith(
+        developerPlatformClient,
+        expectedSampleWebhookVariables,
+        anOrganizationId,
+      )
       expect(triggerLocalWebhook).toHaveBeenCalledWith(aFullLocalAddress, samplePayload, sampleHeaders)
       expect(consoleError).toHaveBeenCalledWith('Localhost delivery failed')
     })
@@ -232,9 +249,9 @@ describe('webhookTriggerService', () => {
     vi.mocked(requestTopics).mockResolvedValue([topic])
   }
 
-  function expectCalls(version: string) {
-    expect(requestApiVersions).toHaveBeenCalledWith(developerPlatformClient)
-    expect(requestTopics).toHaveBeenCalledWith(developerPlatformClient, version)
+  function expectCalls(version: string, organizationId: string) {
+    expect(requestApiVersions).toHaveBeenCalledWith(developerPlatformClient, organizationId)
+    expect(requestTopics).toHaveBeenCalledWith(developerPlatformClient, version, organizationId)
   }
 
   function sampleFlags(): WebhookTriggerInput {
@@ -247,6 +264,7 @@ describe('webhookTriggerService', () => {
       address: anAddress,
       developerPlatformClient,
       path: '.',
+      organizationId: anOrganizationId,
     }
 
     return flags
@@ -262,6 +280,7 @@ describe('webhookTriggerService', () => {
       address: anEventBridgeAddress,
       developerPlatformClient,
       path: '.',
+      organizationId: anOrganizationId,
     }
 
     return flags
@@ -277,6 +296,7 @@ describe('webhookTriggerService', () => {
       address: aFullLocalAddress,
       developerPlatformClient,
       path: '.',
+      organizationId: anOrganizationId,
     }
 
     return flags
diff --git a/packages/app/src/cli/services/webhook/trigger.ts b/packages/app/src/cli/services/webhook/trigger.ts
index cac19d272dc..035dbb6d0fd 100644
--- a/packages/app/src/cli/services/webhook/trigger.ts
+++ b/packages/app/src/cli/services/webhook/trigger.ts
@@ -19,6 +19,7 @@ export interface WebhookTriggerInput {
   clientSecret?: string
   path: string
   config?: string
+  organizationId: string
 }
 
 interface WebhookTriggerOptions {
@@ -29,6 +30,7 @@ interface WebhookTriggerOptions {
   clientSecret: string
   apiKey?: string
   developerPlatformClient: DeveloperPlatformClient
+  organizationId: string
 }
 
 /**
@@ -45,8 +47,8 @@ export async function webhookTriggerService(input: WebhookTriggerInput) {
 }
 
 async function validateAndCollectFlags(input: WebhookTriggerInput): Promise<WebhookTriggerOptions> {
-  const apiVersion = await collectApiVersion(input.developerPlatformClient, input.apiVersion)
-  const topic = await collectTopic(input.developerPlatformClient, apiVersion, input.topic)
+  const apiVersion = await collectApiVersion(input.developerPlatformClient, input.apiVersion, input.organizationId)
+  const topic = await collectTopic(input.developerPlatformClient, apiVersion, input.topic, input.organizationId)
   const [address, deliveryMethod] = await collectAddressAndMethod(input.deliveryMethod, input.address)
   const clientCredentials = await collectCredentials(input, deliveryMethod)
 
@@ -58,6 +60,7 @@ async function validateAndCollectFlags(input: WebhookTriggerInput): Promise<Webh
     apiKey: clientCredentials.apiKey,
     clientSecret: clientCredentials.clientSecret,
     developerPlatformClient: input.developerPlatformClient,
+    organizationId: input.organizationId,
   }
 }
 
@@ -70,7 +73,7 @@ async function sendSample(options: WebhookTriggerOptions) {
     shared_secret: options.clientSecret,
     api_key: options.apiKey,
   }
-  const sample = await getWebhookSample(options.developerPlatformClient, variables)
+  const sample = await getWebhookSample(options.developerPlatformClient, variables, options.organizationId)
 
   if (!sample.success) {
     consoleError(`Request errors:\n${formatErrors(sample.userErrors)}`)
diff --git a/packages/app/src/cli/utilities/developer-platform-client.ts b/packages/app/src/cli/utilities/developer-platform-client.ts
index 87bf8a14bb4..9aab9a65acf 100644
--- a/packages/app/src/cli/utilities/developer-platform-client.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client.ts
@@ -241,9 +241,9 @@ export interface DeveloperPlatformClient {
   ) => Promise<ConvertDevToTransferDisabledSchema>
   updateDeveloperPreview: (input: DevelopmentStorePreviewUpdateInput) => Promise<DevelopmentStorePreviewUpdateSchema>
   appPreviewMode: (input: FindAppPreviewModeVariables) => Promise<FindAppPreviewModeSchema>
-  sendSampleWebhook: (input: SendSampleWebhookVariables) => Promise<SendSampleWebhookSchema>
-  apiVersions: () => Promise<PublicApiVersionsSchema>
-  topics: (input: WebhookTopicsVariables) => Promise<WebhookTopicsSchema>
+  sendSampleWebhook: (input: SendSampleWebhookVariables, organizationId: string) => Promise<SendSampleWebhookSchema>
+  apiVersions: (organizationId: string) => Promise<PublicApiVersionsSchema>
+  topics: (input: WebhookTopicsVariables, organizationId: string) => Promise<WebhookTopicsSchema>
   migrateFlowExtension: (input: MigrateFlowExtensionVariables) => Promise<MigrateFlowExtensionSchema>
   migrateAppModule: (input: MigrateAppModuleVariables) => Promise<MigrateAppModuleSchema>
   updateURLs: (input: UpdateURLsVariables) => Promise<UpdateURLsSchema>
diff --git a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.test.ts b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.test.ts
index c49525391d7..84f17cb74b5 100644
--- a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.test.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.test.ts
@@ -10,6 +10,10 @@ import {OrganizationBetaFlagsQuerySchema} from './app-management-client/graphql/
 import {testUIExtension, testRemoteExtensionTemplates, testOrganizationApp} from '../../models/app/app.test-data.js'
 import {ExtensionInstance} from '../../models/extensions/extension-instance.js'
 import {ListApps} from '../../api/graphql/app-management/generated/apps.js'
+import {PublicApiVersionsQuery} from '../../api/graphql/webhooks/generated/public-api-versions.js'
+import {AvailableTopicsQuery} from '../../api/graphql/webhooks/generated/available-topics.js'
+import {CliTesting, CliTestingMutation} from '../../api/graphql/webhooks/generated/cli-testing.js'
+import {SendSampleWebhookVariables} from '../../services/webhook/request-sample.js'
 import {describe, expect, test, vi} from 'vitest'
 import {CLI_KIT_VERSION} from '@shopify/cli-kit/common/version'
 import {fetch} from '@shopify/cli-kit/node/http'
@@ -17,10 +21,12 @@ import {businessPlatformOrganizationsRequest} from '@shopify/cli-kit/node/api/bu
 import {appManagementRequestDoc} from '@shopify/cli-kit/node/api/app-management'
 import {BugError} from '@shopify/cli-kit/node/error'
 import {randomUUID} from '@shopify/cli-kit/node/crypto'
+import {webhooksRequest} from '@shopify/cli-kit/node/api/webhooks'
 
 vi.mock('@shopify/cli-kit/node/http')
 vi.mock('@shopify/cli-kit/node/api/business-platform')
 vi.mock('@shopify/cli-kit/node/api/app-management')
+vi.mock('@shopify/cli-kit/node/api/webhooks')
 
 const extensionA = await testUIExtension({uid: 'extension-a-uuid'})
 const extensionB = await testUIExtension({uid: 'extension-b-uuid'})
@@ -288,3 +294,177 @@ describe('searching for apps', () => {
     await expect(client.appsForOrg(orgId)).rejects.toThrow(BugError)
   })
 })
+
+describe('apiVersions', () => {
+  test('fetches available public API versions', async () => {
+    // Given
+    const orgId = '1'
+    const mockedResponse: PublicApiVersionsQuery = {
+      publicApiVersions: [{handle: '2024-07'}, {handle: '2024-10'}, {handle: '2025-01'}, {handle: 'unstable'}],
+    }
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve('token')
+    const apiVersions = await client.apiVersions(orgId)
+
+    // Then
+    expect(apiVersions.publicApiVersions.length).toEqual(mockedResponse.publicApiVersions.length)
+    expect(apiVersions.publicApiVersions).toEqual(mockedResponse.publicApiVersions.map((version) => version.handle))
+  })
+})
+
+describe('topics', () => {
+  test('fetches available topics for a valid API version', async () => {
+    // Given
+    const orgId = '1'
+    const mockedResponse: AvailableTopicsQuery = {availableTopics: ['app/uninstalled', 'products/created']}
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve('token')
+    const topics = await client.topics({api_version: '2024-07'}, orgId)
+
+    // Then
+    expect(topics.webhookTopics.length).toEqual(mockedResponse.availableTopics?.length)
+    expect(topics.webhookTopics).toEqual(mockedResponse.availableTopics)
+  })
+
+  test('returns an empty list when failing', async () => {
+    // Given
+    const orgId = '1'
+    const mockedResponse: AvailableTopicsQuery = {availableTopics: null}
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve('token')
+    const topics = await client.topics({api_version: 'invalid'}, orgId)
+
+    // Then
+    expect(topics.webhookTopics.length).toEqual(0)
+  })
+})
+
+describe('sendSampleWebhook', () => {
+  test('succeeds for local delivery', async () => {
+    // Given
+    const orgId = '1'
+    const input: SendSampleWebhookVariables = {
+      address: 'http://localhost:3000/webhooks',
+      api_key: 'abc123',
+      api_version: '2025-01',
+      delivery_method: 'localhost',
+      shared_secret: 'secret',
+      topic: 'app/uninstalled',
+    }
+    const mockedResponse: CliTestingMutation = {
+      cliTesting: {
+        headers: `{"Content-Type":"application/json"}`,
+        samplePayload: `{"id": 42,"name":"test"}`,
+        success: true,
+        errors: [],
+      },
+    }
+    const expectedVariables = {
+      address: input.address,
+      apiKey: input.api_key,
+      apiVersion: input.api_version,
+      deliveryMethod: input.delivery_method,
+      sharedSecret: input.shared_secret,
+      topic: input.topic,
+    }
+    const token = 'token'
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve(token)
+    const result = await client.sendSampleWebhook(input, orgId)
+
+    // Then
+    expect(webhooksRequest).toHaveBeenCalledWith(orgId, CliTesting, token, expectedVariables)
+    expect(result.sendSampleWebhook.samplePayload).toEqual(mockedResponse.cliTesting?.samplePayload)
+    expect(result.sendSampleWebhook.headers).toEqual(mockedResponse.cliTesting?.headers)
+    expect(result.sendSampleWebhook.success).toEqual(true)
+    expect(result.sendSampleWebhook.userErrors).toEqual([])
+  })
+
+  test('succeeds for remote delivery', async () => {
+    // Given
+    const orgId = '1'
+    const input: SendSampleWebhookVariables = {
+      address: 'https://webhooks.test',
+      api_key: 'abc123',
+      api_version: '2025-01',
+      delivery_method: 'http',
+      shared_secret: 'secret',
+      topic: 'app/uninstalled',
+    }
+    const mockedResponse: CliTestingMutation = {
+      cliTesting: {
+        headers: '{}',
+        samplePayload: '{}',
+        success: true,
+        errors: [],
+      },
+    }
+    const expectedVariables = {
+      address: input.address,
+      apiKey: input.api_key,
+      apiVersion: input.api_version,
+      deliveryMethod: input.delivery_method,
+      sharedSecret: input.shared_secret,
+      topic: input.topic,
+    }
+    const token = 'token'
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve(token)
+    const result = await client.sendSampleWebhook(input, orgId)
+
+    // Then
+    expect(webhooksRequest).toHaveBeenCalledWith(orgId, CliTesting, token, expectedVariables)
+    expect(result.sendSampleWebhook.samplePayload).toEqual('{}')
+    expect(result.sendSampleWebhook.headers).toEqual('{}')
+    expect(result.sendSampleWebhook.success).toEqual(true)
+    expect(result.sendSampleWebhook.userErrors).toEqual([])
+  })
+
+  test('handles API failures', async () => {
+    // Given
+    const orgId = '1'
+    const input: SendSampleWebhookVariables = {
+      address: 'https://webhooks.test',
+      api_key: 'abc123',
+      api_version: 'invalid',
+      delivery_method: 'http',
+      shared_secret: 'secret',
+      topic: 'app/uninstalled',
+    }
+    const mockedResponse: CliTestingMutation = {
+      cliTesting: {
+        headers: '{}',
+        samplePayload: '{}',
+        success: false,
+        errors: ['Invalid api_version'],
+      },
+    }
+    vi.mocked(webhooksRequest).mockResolvedValueOnce(mockedResponse)
+
+    // When
+    const client = new AppManagementClient()
+    client.token = () => Promise.resolve('token')
+    const result = await client.sendSampleWebhook(input, orgId)
+
+    // Then
+    expect(result.sendSampleWebhook.samplePayload).toEqual('{}')
+    expect(result.sendSampleWebhook.headers).toEqual('{}')
+    expect(result.sendSampleWebhook.success).toEqual(false)
+    expect(result.sendSampleWebhook.userErrors).toEqual([{message: 'Invalid api_version', fields: []}])
+  })
+})
diff --git a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
index ab875512679..cd76748a4c9 100644
--- a/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client/app-management-client.ts
@@ -46,7 +46,11 @@ import {
 } from '../../api/graphql/development_preview.js'
 import {AppReleaseSchema} from '../../api/graphql/app_release.js'
 import {AppVersionsDiffSchema} from '../../api/graphql/app_versions_diff.js'
-import {SendSampleWebhookSchema, SendSampleWebhookVariables} from '../../services/webhook/request-sample.js'
+import {
+  SampleWebhook,
+  SendSampleWebhookSchema,
+  SendSampleWebhookVariables,
+} from '../../services/webhook/request-sample.js'
 import {PublicApiVersionsSchema} from '../../services/webhook/request-api-versions.js'
 import {WebhookTopicsSchema, WebhookTopicsVariables} from '../../services/webhook/request-topics.js'
 import {
@@ -100,6 +104,9 @@ import {FetchSpecifications} from '../../api/graphql/app-management/generated/sp
 import {ListApps} from '../../api/graphql/app-management/generated/apps.js'
 import {FindOrganizations} from '../../api/graphql/business-platform-destinations/generated/find-organizations.js'
 import {UserInfo} from '../../api/graphql/business-platform-destinations/generated/user-info.js'
+import {AvailableTopics} from '../../api/graphql/webhooks/generated/available-topics.js'
+import {CliTesting} from '../../api/graphql/webhooks/generated/cli-testing.js'
+import {PublicApiVersions} from '../../api/graphql/webhooks/generated/public-api-versions.js'
 import {ensureAuthenticatedAppManagement, ensureAuthenticatedBusinessPlatform} from '@shopify/cli-kit/node/session'
 import {isUnitTest} from '@shopify/cli-kit/node/context/local'
 import {AbortError, BugError} from '@shopify/cli-kit/node/error'
@@ -115,6 +122,7 @@ import {CLI_KIT_VERSION} from '@shopify/cli-kit/common/version'
 import {versionSatisfies} from '@shopify/cli-kit/node/node-package-manager'
 import {outputDebug} from '@shopify/cli-kit/node/output'
 import {developerDashboardFqdn} from '@shopify/cli-kit/node/context/fqdn'
+import {webhooksRequest} from '@shopify/cli-kit/node/api/webhooks'
 
 const TEMPLATE_JSON_URL = 'https://cdn.shopify.com/static/cli/extensions/templates.json'
 
@@ -709,25 +717,46 @@ export class AppManagementClient implements DeveloperPlatformClient {
     throw new BugError('Not implemented: appPreviewMode')
   }
 
-  async sendSampleWebhook(_input: SendSampleWebhookVariables): Promise<SendSampleWebhookSchema> {
-    outputDebug('⚠️ sendSampleWebhook is not implemented')
-    return {
-      sendSampleWebhook: {
-        samplePayload: '',
-        headers: '{}',
-        success: true,
-        userErrors: [],
-      },
+  async sendSampleWebhook(input: SendSampleWebhookVariables, organizationId: string): Promise<SendSampleWebhookSchema> {
+    const query = CliTesting
+    const variables = {
+      address: input.address,
+      apiKey: input.api_key,
+      apiVersion: input.api_version,
+      deliveryMethod: input.delivery_method,
+      sharedSecret: input.shared_secret,
+      topic: input.topic,
+    }
+    const result = await webhooksRequest(organizationId, query, await this.token(), variables)
+    let sendSampleWebhook: SampleWebhook = {samplePayload: '{}', headers: '{}', success: false, userErrors: []}
+    const cliTesting = result.cliTesting
+    if (cliTesting) {
+      sendSampleWebhook = {
+        samplePayload: cliTesting.samplePayload ?? '{}',
+        headers: cliTesting.headers ?? '{}',
+        success: cliTesting.success,
+        userErrors: cliTesting.errors.map((error) => ({message: error, fields: []})),
+      }
     }
+    return {sendSampleWebhook}
   }
 
-  async apiVersions(): Promise<PublicApiVersionsSchema> {
-    outputDebug('⚠️ apiVersions is not implemented')
-    return {publicApiVersions: ['unstable']}
+  async apiVersions(organizationId: string): Promise<PublicApiVersionsSchema> {
+    const result = await webhooksRequest(organizationId, PublicApiVersions, await this.token(), {})
+    return {publicApiVersions: result.publicApiVersions.map((version) => version.handle)}
   }
 
-  async topics(_input: WebhookTopicsVariables): Promise<WebhookTopicsSchema> {
-    throw new BugError('Not implemented: topics')
+  async topics(
+    {api_version: apiVersion}: WebhookTopicsVariables,
+    organizationId: string,
+  ): Promise<WebhookTopicsSchema> {
+    const query = AvailableTopics
+    const variables = {apiVersion}
+    const result = await webhooksRequest(organizationId, query, await this.token(), variables)
+
+    return {
+      webhookTopics: result.availableTopics ?? [],
+    }
   }
 
   async migrateFlowExtension(_input: MigrateFlowExtensionVariables): Promise<MigrateFlowExtensionSchema> {
diff --git a/packages/app/src/cli/utilities/developer-platform-client/partners-client.ts b/packages/app/src/cli/utilities/developer-platform-client/partners-client.ts
index f25f50b35d0..0db97d7b026 100644
--- a/packages/app/src/cli/utilities/developer-platform-client/partners-client.ts
+++ b/packages/app/src/cli/utilities/developer-platform-client/partners-client.ts
@@ -474,15 +474,18 @@ export class PartnersClient implements DeveloperPlatformClient {
     return this.request(FindAppPreviewModeQuery, input)
   }
 
-  async sendSampleWebhook(input: SendSampleWebhookVariables): Promise<SendSampleWebhookSchema> {
+  async sendSampleWebhook(
+    input: SendSampleWebhookVariables,
+    _organizationId: string,
+  ): Promise<SendSampleWebhookSchema> {
     return this.request(sendSampleWebhookMutation, input)
   }
 
-  async apiVersions(): Promise<PublicApiVersionsSchema> {
+  async apiVersions(_organizationId: string): Promise<PublicApiVersionsSchema> {
     return this.request(GetApiVersionsQuery)
   }
 
-  async topics(input: WebhookTopicsVariables): Promise<WebhookTopicsSchema> {
+  async topics(input: WebhookTopicsVariables, _organizationId: string): Promise<WebhookTopicsSchema> {
     return this.request(getTopicsQuery, input)
   }
 
diff --git a/packages/cli-kit/src/public/node/api/webhooks.ts b/packages/cli-kit/src/public/node/api/webhooks.ts
new file mode 100644
index 00000000000..07f67cf6e19
--- /dev/null
+++ b/packages/cli-kit/src/public/node/api/webhooks.ts
@@ -0,0 +1,45 @@
+import {graphqlRequestDoc} from './graphql.js'
+import {appManagementFqdn} from '../context/fqdn.js'
+import Bottleneck from 'bottleneck'
+import {Variables} from 'graphql-request'
+import {TypedDocumentNode} from '@graphql-typed-document-node/core'
+
+// API Rate limiter
+// Jobs are launched every 150ms
+// Only 10 requests can be executed concurrently.
+const limiter = new Bottleneck({
+  minTime: 150,
+  maxConcurrent: 10,
+})
+
+/**
+ * Executes an org-scoped GraphQL query against the App Management API.
+ * Uses typed documents.
+ *
+ * @param organizationId - Organization ID required to check permissions.
+ * @param query - GraphQL query to execute.
+ * @param token - Partners token.
+ * @param variables - GraphQL variables to pass to the query.
+ * @returns The response of the query of generic type <T>.
+ */
+export async function webhooksRequest<TResult, TVariables extends Variables>(
+  organizationId: string,
+  query: TypedDocumentNode<TResult, TVariables>,
+  token: string,
+  variables?: TVariables,
+): Promise<TResult> {
+  const api = 'Webhooks'
+  const fqdn = await appManagementFqdn()
+  const url = `https://${fqdn}/webhooks/unstable/organizations/${organizationId}/graphql.json`
+  const result = limiter.schedule<TResult>(() =>
+    graphqlRequestDoc<TResult, TVariables>({
+      query,
+      api,
+      url,
+      token,
+      variables,
+    }),
+  )
+
+  return result
+}