diff --git a/packages/driver/src/cypress/error_messages.ts b/packages/driver/src/cypress/error_messages.ts
index 9287733b8cd..7b2cb435cb5 100644
--- a/packages/driver/src/cypress/error_messages.ts
+++ b/packages/driver/src/cypress/error_messages.ts
@@ -1340,7 +1340,7 @@ export default {
         message: stripIndent`\
         Timed out waiting for cy.prompt Cloud code:
 
-        - ${obj.error.code}: ${obj.error.message}
+        - ${obj.error.code ? `${obj.error.code}: ` : ''}${obj.error.message}
 
          Check your network connection and system configuration.
       `,
diff --git a/packages/server/lib/cloud/api/cy-prompt/get_cy_prompt_bundle.ts b/packages/server/lib/cloud/api/cy-prompt/get_cy_prompt_bundle.ts
index 0eb3f3879af..7c0c4c14e5c 100644
--- a/packages/server/lib/cloud/api/cy-prompt/get_cy_prompt_bundle.ts
+++ b/packages/server/lib/cloud/api/cy-prompt/get_cy_prompt_bundle.ts
@@ -10,8 +10,9 @@ import { verifySignatureFromFile } from '../../encryption'
 const pkg = require('@packages/root')
 const _delay = linearDelay(500)
 
-export const getCyPromptBundle = async ({ cyPromptUrl, projectId, bundlePath }: { cyPromptUrl: string, projectId?: string, bundlePath: string }) => {
+export const getCyPromptBundle = async ({ cyPromptUrl, projectId, bundlePath }: { cyPromptUrl: string, projectId?: string, bundlePath: string }): Promise<string> => {
   let responseSignature: string | null = null
+  let responseManifestSignature: string | null = null
 
   await (asyncRetry(async () => {
     const response = await fetch(cyPromptUrl, {
@@ -34,6 +35,7 @@ export const getCyPromptBundle = async ({ cyPromptUrl, projectId, bundlePath }:
     }
 
     responseSignature = response.headers.get('x-cypress-signature')
+    responseManifestSignature = response.headers.get('x-cypress-manifest-signature')
 
     await new Promise<void>((resolve, reject) => {
       const writeStream = createWriteStream(bundlePath)
@@ -56,9 +58,15 @@ export const getCyPromptBundle = async ({ cyPromptUrl, projectId, bundlePath }:
     throw new Error('Unable to get cy-prompt signature')
   }
 
+  if (!responseManifestSignature) {
+    throw new Error('Unable to get cy-prompt manifest signature')
+  }
+
   const verified = await verifySignatureFromFile(bundlePath, responseSignature)
 
   if (!verified) {
     throw new Error('Unable to verify cy-prompt signature')
   }
+
+  return responseManifestSignature
 }
diff --git a/packages/server/lib/cloud/cy-prompt/CyPromptLifecycleManager.ts b/packages/server/lib/cloud/cy-prompt/CyPromptLifecycleManager.ts
index 2809e815d7f..27773c6f103 100644
--- a/packages/server/lib/cloud/cy-prompt/CyPromptLifecycleManager.ts
+++ b/packages/server/lib/cloud/cy-prompt/CyPromptLifecycleManager.ts
@@ -13,11 +13,12 @@ import { ensureCyPromptBundle } from './ensure_cy_prompt_bundle'
 import chokidar from 'chokidar'
 import { getCloudMetadata } from '../get_cloud_metadata'
 import type { CyPromptAuthenticatedUserShape } from '@packages/types'
+import crypto from 'crypto'
 
 const debug = Debug('cypress:server:cy-prompt-lifecycle-manager')
 
 export class CyPromptLifecycleManager {
-  private static hashLoadingMap: Map<string, Promise<void>> = new Map()
+  private static hashLoadingMap: Map<string, Promise<Record<string, string>>> = new Map()
   private static watcher: chokidar.FSWatcher | null = null
   private cyPromptManagerPromise?: Promise<{
     cyPromptManager?: CyPromptManager
@@ -124,6 +125,7 @@ export class CyPromptLifecycleManager {
   }): Promise<{ cyPromptManager?: CyPromptManager, error?: Error }> {
     let cyPromptHash: string
     let cyPromptPath: string
+    let manifest: Record<string, string>
 
     const currentProjectOptions = await getProjectOptions()
     const projectId = currentProjectOptions.projectSlug
@@ -148,15 +150,30 @@ export class CyPromptLifecycleManager {
         CyPromptLifecycleManager.hashLoadingMap.set(cyPromptHash, hashLoadingPromise)
       }
 
-      await hashLoadingPromise
+      manifest = await hashLoadingPromise
     } else {
       cyPromptPath = process.env.CYPRESS_LOCAL_CY_PROMPT_PATH
       cyPromptHash = 'local'
+      manifest = {}
     }
 
     const serverFilePath = path.join(cyPromptPath, 'server', 'index.js')
 
     const script = await readFile(serverFilePath, 'utf8')
+
+    if (!process.env.CYPRESS_LOCAL_CY_PROMPT_PATH) {
+      const expectedHash = manifest[path.posix.join('server', 'index.js')]
+      const actualHash = crypto.createHash('sha256').update(script).digest('hex')
+
+      if (!expectedHash) {
+        throw new Error('Expected hash for cy prompt server script not found in manifest')
+      }
+
+      if (actualHash !== expectedHash) {
+        throw new Error('Invalid hash for cy prompt server script')
+      }
+    }
+
     const cyPromptManager = new CyPromptManager()
 
     const { cloudUrl } = await getCloudMetadata(cloudDataSource)
@@ -172,6 +189,7 @@ export class CyPromptLifecycleManager {
         asyncRetry,
       },
       getProjectOptions,
+      manifest,
     })
 
     debug('cy prompt is ready')
diff --git a/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts b/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
index 7b72d466f7a..89d786275bb 100644
--- a/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
+++ b/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
@@ -3,6 +3,7 @@ import type { Router } from 'express'
 import Debug from 'debug'
 import { requireScript } from '../require_script'
 import type { Socket } from 'socket.io'
+import crypto, { BinaryLike } from 'crypto'
 
 interface CyPromptServer { default: CyPromptServerDefaultShape }
 
@@ -18,6 +19,7 @@ interface SetupOptions {
     record?: boolean
     key?: string
   }>
+  manifest: Record<string, string>
 }
 
 const debug = Debug('cypress:server:cy-prompt')
@@ -26,7 +28,7 @@ export class CyPromptManager implements CyPromptManagerShape {
   status: CyPromptStatus = 'NOT_INITIALIZED'
   private _cyPromptServer: CyPromptServerShape | undefined
 
-  async setup ({ script, cyPromptPath, cyPromptHash, getProjectOptions, cloudApi }: SetupOptions): Promise<void> {
+  async setup ({ script, cyPromptPath, cyPromptHash, getProjectOptions, cloudApi, manifest }: SetupOptions): Promise<void> {
     const { createCyPromptServer } = requireScript<CyPromptServer>(script).default
 
     this._cyPromptServer = await createCyPromptServer({
@@ -34,6 +36,18 @@ export class CyPromptManager implements CyPromptManagerShape {
       cyPromptPath,
       cloudApi,
       getProjectOptions,
+      manifest,
+      verifyHash: (contents: BinaryLike, expectedHash: string) => {
+        // If we are running locally, we don't need to verify the signature. This
+        // environment variable will get stripped in the binary.
+        if (process.env.CYPRESS_LOCAL_CY_PROMPT_PATH) {
+          return true
+        }
+
+        const actualHash = crypto.createHash('sha256').update(contents).digest('hex')
+
+        return actualHash === expectedHash
+      },
     })
 
     this.status = 'INITIALIZED'
diff --git a/packages/server/lib/cloud/cy-prompt/ensure_cy_prompt_bundle.ts b/packages/server/lib/cloud/cy-prompt/ensure_cy_prompt_bundle.ts
index 8691fbea863..717095c0de2 100644
--- a/packages/server/lib/cloud/cy-prompt/ensure_cy_prompt_bundle.ts
+++ b/packages/server/lib/cloud/cy-prompt/ensure_cy_prompt_bundle.ts
@@ -1,8 +1,9 @@
-import { remove, ensureDir } from 'fs-extra'
+import { remove, ensureDir, readFile, pathExists } from 'fs-extra'
 
 import tar from 'tar'
 import { getCyPromptBundle } from '../api/cy-prompt/get_cy_prompt_bundle'
 import path from 'path'
+import { verifySignature } from '../encryption'
 
 const DOWNLOAD_TIMEOUT = 30000
 
@@ -21,7 +22,7 @@ interface EnsureCyPromptBundleOptions {
  * @param options.projectId - The project ID of the cy prompt bundle
  * @param options.downloadTimeoutMs - The timeout for the cy prompt bundle download
  */
-export const ensureCyPromptBundle = async ({ cyPromptPath, cyPromptUrl, projectId, downloadTimeoutMs = DOWNLOAD_TIMEOUT }: EnsureCyPromptBundleOptions) => {
+export const ensureCyPromptBundle = async ({ cyPromptPath, cyPromptUrl, projectId, downloadTimeoutMs = DOWNLOAD_TIMEOUT }: EnsureCyPromptBundleOptions): Promise<Record<string, string>> => {
   const bundlePath = path.join(cyPromptPath, 'bundle.tar')
 
   // First remove cyPromptPath to ensure we have a clean slate
@@ -30,7 +31,7 @@ export const ensureCyPromptBundle = async ({ cyPromptPath, cyPromptUrl, projectI
 
   let timeoutId: NodeJS.Timeout
 
-  await Promise.race([
+  const responseManifestSignature: string = await Promise.race([
     getCyPromptBundle({
       cyPromptUrl,
       projectId,
@@ -43,10 +44,26 @@ export const ensureCyPromptBundle = async ({ cyPromptPath, cyPromptUrl, projectI
     }),
   ]).finally(() => {
     clearTimeout(timeoutId)
-  })
+  }) as string
 
   await tar.extract({
     file: bundlePath,
     cwd: cyPromptPath,
   })
+
+  const manifestPath = path.join(cyPromptPath, 'manifest.json')
+
+  if (!(await pathExists(manifestPath))) {
+    throw new Error('Unable to find cy-prompt manifest')
+  }
+
+  const manifestContents = await readFile(manifestPath, 'utf8')
+
+  const verified = await verifySignature(manifestContents, responseManifestSignature)
+
+  if (!verified) {
+    throw new Error('Unable to verify cy-prompt signature')
+  }
+
+  return JSON.parse(manifestContents)
 }
diff --git a/packages/server/lib/cloud/encryption.ts b/packages/server/lib/cloud/encryption.ts
index 3fee7eeff6e..5f62572b368 100644
--- a/packages/server/lib/cloud/encryption.ts
+++ b/packages/server/lib/cloud/encryption.ts
@@ -1,4 +1,4 @@
-import crypto from 'crypto'
+import crypto, { BinaryLike } from 'crypto'
 import { TextEncoder, promisify } from 'util'
 import { generalDecrypt, GeneralJWE } from 'jose'
 import base64Url from 'base64url'
@@ -37,7 +37,7 @@ export interface EncryptRequestData {
   secretKey: crypto.KeyObject
 }
 
-export function verifySignature (body: string, signature: string, publicKey?: crypto.KeyObject) {
+export function verifySignature (body: BinaryLike, signature: string, publicKey?: crypto.KeyObject) {
   const verify = crypto.createVerify('SHA256')
 
   verify.update(body)
diff --git a/packages/server/test/unit/cloud/api/cy-prompt/get_cy_prompt_bundle_spec.ts b/packages/server/test/unit/cloud/api/cy-prompt/get_cy_prompt_bundle_spec.ts
index 35fe19437b0..c5e1f4ee265 100644
--- a/packages/server/test/unit/cloud/api/cy-prompt/get_cy_prompt_bundle_spec.ts
+++ b/packages/server/test/unit/cloud/api/cy-prompt/get_cy_prompt_bundle_spec.ts
@@ -31,15 +31,15 @@ describe('getCyPromptBundle', () => {
         createWriteStream: createWriteStreamStub,
       },
       'cross-fetch': crossFetchStub,
-      '../../encryption': {
-        verifySignatureFromFile: verifySignatureFromFileStub,
-      },
       'os': {
         platform: () => 'linux',
       },
       '@packages/root': {
         version: '1.2.3',
       },
+      '../../encryption': {
+        verifySignatureFromFile: verifySignatureFromFileStub,
+      },
     }).getCyPromptBundle
   })
 
@@ -53,6 +53,10 @@ describe('getCyPromptBundle', () => {
           if (header === 'x-cypress-signature') {
             return '159'
           }
+
+          if (header === 'x-cypress-manifest-signature') {
+            return '160'
+          }
         },
       },
     })
@@ -61,7 +65,7 @@ describe('getCyPromptBundle', () => {
 
     const projectId = '12345'
 
-    await getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })
+    const responseSignature = await getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })
 
     expect(crossFetchStub).to.be.calledWith('http://localhost:1234/cy-prompt/bundle/abc.tgz', {
       agent: sinon.match.any,
@@ -80,6 +84,8 @@ describe('getCyPromptBundle', () => {
     expect(writeResult).to.eq('console.log("cy-prompt script")')
 
     expect(verifySignatureFromFileStub).to.be.calledWith('/tmp/cypress/cy-prompt/abc/bundle.tar', '159')
+
+    expect(responseSignature).to.eq('160')
   })
 
   it('downloads the cy-prompt bundle and extracts it after 1 fetch failure', async () => {
@@ -93,6 +99,10 @@ describe('getCyPromptBundle', () => {
           if (header === 'x-cypress-signature') {
             return '159'
           }
+
+          if (header === 'x-cypress-manifest-signature') {
+            return '160'
+          }
         },
       },
     })
@@ -101,7 +111,7 @@ describe('getCyPromptBundle', () => {
 
     const projectId = '12345'
 
-    await getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })
+    const responseSignature = await getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })
 
     expect(crossFetchStub).to.be.calledWith('http://localhost:1234/cy-prompt/bundle/abc.tgz', {
       agent: sinon.match.any,
@@ -120,6 +130,8 @@ describe('getCyPromptBundle', () => {
     expect(writeResult).to.eq('console.log("cy-prompt script")')
 
     expect(verifySignatureFromFileStub).to.be.calledWith('/tmp/cypress/cy-prompt/abc/bundle.tar', '159')
+
+    expect(responseSignature).to.eq('160')
   })
 
   it('throws an error and returns a cy-prompt manager in error state if the fetch fails more than twice', async () => {
@@ -184,6 +196,10 @@ describe('getCyPromptBundle', () => {
           if (header === 'x-cypress-signature') {
             return '159'
           }
+
+          if (header === 'x-cypress-manifest-signature') {
+            return '160'
+          }
         },
       },
     })
@@ -219,13 +235,50 @@ describe('getCyPromptBundle', () => {
       statusText: 'OK',
       body: readStream,
       headers: {
-        get: () => null,
+        get: (header) => {
+          if (header === 'x-cypress-manifest-signature') {
+            return '160'
+          }
+        },
       },
     })
 
     const projectId = '12345'
 
-    await expect(getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })).to.be.rejected
+    await expect(getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })).to.be.rejectedWith('Unable to get cy-prompt signature')
+
+    expect(crossFetchStub).to.be.calledWith('http://localhost:1234/cy-prompt/bundle/abc.tgz', {
+      agent: sinon.match.any,
+      method: 'GET',
+      headers: {
+        'x-route-version': '1',
+        'x-cypress-signature': '1',
+        'x-cypress-project-slug': '12345',
+        'x-cypress-cy-prompt-mount-version': '1',
+        'x-os-name': 'linux',
+        'x-cypress-version': '1.2.3',
+      },
+      encrypt: 'signed',
+    })
+  })
+
+  it('throws an error if there is no manifest signature in the response headers', async () => {
+    crossFetchStub.resolves({
+      ok: true,
+      statusText: 'OK',
+      body: readStream,
+      headers: {
+        get: (header) => {
+          if (header === 'x-cypress-signature') {
+            return '159'
+          }
+        },
+      },
+    })
+
+    const projectId = '12345'
+
+    await expect(getCyPromptBundle({ cyPromptUrl: 'http://localhost:1234/cy-prompt/bundle/abc.tgz', projectId, bundlePath: '/tmp/cypress/cy-prompt/abc/bundle.tar' })).to.be.rejectedWith('Unable to get cy-prompt manifest signature')
 
     expect(crossFetchStub).to.be.calledWith('http://localhost:1234/cy-prompt/bundle/abc.tgz', {
       agent: sinon.match.any,
diff --git a/packages/server/test/unit/cloud/cy-prompt/CyPromptLifecycleManager_spec.ts b/packages/server/test/unit/cloud/cy-prompt/CyPromptLifecycleManager_spec.ts
index 091d9fd0081..311baa4a1db 100644
--- a/packages/server/test/unit/cloud/cy-prompt/CyPromptLifecycleManager_spec.ts
+++ b/packages/server/test/unit/cloud/cy-prompt/CyPromptLifecycleManager_spec.ts
@@ -24,6 +24,7 @@ describe('CyPromptLifecycleManager', () => {
   let watcherStub: sinon.SinonStub = sinon.stub()
   let watcherOnStub: sinon.SinonStub = sinon.stub()
   let watcherCloseStub: sinon.SinonStub = sinon.stub()
+  const mockContents: string = 'console.log("cy-prompt script")'
 
   beforeEach(() => {
     postCyPromptSessionStub = sinon.stub()
@@ -51,7 +52,7 @@ describe('CyPromptLifecycleManager', () => {
         },
       },
       'fs-extra': {
-        readFile: readFileStub.resolves('console.log("cy-prompt script")'),
+        readFile: readFileStub.resolves(mockContents),
       },
       'chokidar': {
         watch: watcherStub.returns({
@@ -122,6 +123,12 @@ describe('CyPromptLifecycleManager', () => {
         })
       })
 
+      const mockManifest = {
+        'server/index.js': 'c3c4ab913ca059819549f105e756a4c4471df19abef884ce85eafc7b7970e7b4',
+      }
+
+      ensureCyPromptBundleStub.resolves(mockManifest)
+
       await cyPromptReadyPromise
 
       expect(mockCtx.update).to.be.calledOnce
@@ -142,6 +149,7 @@ describe('CyPromptLifecycleManager', () => {
           asyncRetry,
         },
         getProjectOptions: sinon.match.func,
+        manifest: mockManifest,
       })
 
       expect(postCyPromptSessionStub).to.be.calledWith({
@@ -167,6 +175,12 @@ describe('CyPromptLifecycleManager', () => {
         })
       })
 
+      const mockManifest = {
+        'server/index.js': 'c3c4ab913ca059819549f105e756a4c4471df19abef884ce85eafc7b7970e7b4',
+      }
+
+      ensureCyPromptBundleStub.resolves(mockManifest)
+
       const cyPromptManager1 = await cyPromptReadyPromise1
 
       cyPromptLifecycleManager.initializeCyPromptManager({
@@ -205,6 +219,7 @@ describe('CyPromptLifecycleManager', () => {
           asyncRetry,
         },
         getProjectOptions: sinon.match.func,
+        manifest: mockManifest,
       })
 
       expect(postCyPromptSessionStub).to.be.calledWith({
@@ -248,6 +263,7 @@ describe('CyPromptLifecycleManager', () => {
           asyncRetry,
         },
         getProjectOptions: sinon.match.func,
+        manifest: {},
       })
 
       expect(postCyPromptSessionStub).to.be.calledWith({
@@ -281,6 +297,60 @@ describe('CyPromptLifecycleManager', () => {
       expect(mockCyPromptManagerPromise).to.be.present
       expect(await mockCyPromptManagerPromise).to.equal(updatedCyPromptManager)
     })
+
+    it('throws an error when the cy-prompt server script is not found in the manifest', async () => {
+      cyPromptManagerSetupStub.callsFake((args) => {
+        return Promise.resolve()
+      })
+
+      const mockManifest = {}
+
+      ensureCyPromptBundleStub.resolves(mockManifest)
+
+      cyPromptLifecycleManager.initializeCyPromptManager({
+        cloudDataSource: mockCloudDataSource,
+        ctx: mockCtx,
+        record: false,
+        key: '123e4567-e89b-12d3-a456-426614174000',
+      })
+
+      // @ts-expect-error - accessing private property
+      const cyPromptPromise = cyPromptLifecycleManager.cyPromptManagerPromise
+
+      expect(cyPromptPromise).to.not.be.null
+
+      const { error } = await cyPromptPromise
+
+      expect(error.message).to.equal('Expected hash for cy prompt server script not found in manifest')
+    })
+
+    it('throws an error when the cy-prompt server script is wrong in the manifest', async () => {
+      cyPromptManagerSetupStub.callsFake((args) => {
+        return Promise.resolve()
+      })
+
+      const mockManifest = {
+        'server/index.js': 'a1',
+      }
+
+      ensureCyPromptBundleStub.resolves(mockManifest)
+
+      cyPromptLifecycleManager.initializeCyPromptManager({
+        cloudDataSource: mockCloudDataSource,
+        ctx: mockCtx,
+        record: false,
+        key: '123e4567-e89b-12d3-a456-426614174000',
+      })
+
+      // @ts-expect-error - accessing private property
+      const cyPromptPromise = cyPromptLifecycleManager.cyPromptManagerPromise
+
+      expect(cyPromptPromise).to.not.be.null
+
+      const { error } = await cyPromptPromise
+
+      expect(error.message).to.equal('Invalid hash for cy prompt server script')
+    })
   })
 
   describe('getCyPrompt', () => {
@@ -304,6 +374,14 @@ describe('CyPromptLifecycleManager', () => {
   })
 
   describe('registerCyPromptReadyListener', () => {
+    beforeEach(() => {
+      const mockManifest = {
+        'server/index.js': 'c3c4ab913ca059819549f105e756a4c4471df19abef884ce85eafc7b7970e7b4',
+      }
+
+      ensureCyPromptBundleStub.resolves(mockManifest)
+    })
+
     it('registers a listener that will be called when cy-prompt is ready', () => {
       const listener = sinon.stub()
 
diff --git a/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts b/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
index b56720b915a..7e52fe117be 100644
--- a/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
+++ b/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
@@ -31,6 +31,9 @@ describe('lib/cloud/cy-prompt', () => {
       cyPromptHash: 'abcdefg',
       projectSlug: '1234',
       cloudApi: {} as any,
+      manifest: {
+        'server/index.js': 'abcdefg',
+      },
       getProjectOptions: () => {
         return Promise.resolve({
           user: {
diff --git a/packages/server/test/unit/cloud/cy-prompt/ensure_cy_prompt_bundle_spec.ts b/packages/server/test/unit/cloud/cy-prompt/ensure_cy_prompt_bundle_spec.ts
index cba1100c9df..054db8fb021 100644
--- a/packages/server/test/unit/cloud/cy-prompt/ensure_cy_prompt_bundle_spec.ts
+++ b/packages/server/test/unit/cloud/cy-prompt/ensure_cy_prompt_bundle_spec.ts
@@ -9,12 +9,22 @@ describe('ensureCyPromptBundle', () => {
   let ensureStub: sinon.SinonStub = sinon.stub()
   let extractStub: sinon.SinonStub = sinon.stub()
   let getCyPromptBundleStub: sinon.SinonStub = sinon.stub()
+  let readFileStub: sinon.SinonStub = sinon.stub()
+  let verifySignatureStub: sinon.SinonStub = sinon.stub()
+  let pathExistsStub: sinon.SinonStub = sinon.stub()
+  const mockResponseSignature = '159'
+  const mockManifest = {
+    'server/index.js': 'abcdefg',
+  }
 
   beforeEach(() => {
     rmStub = sinon.stub()
     ensureStub = sinon.stub()
     extractStub = sinon.stub()
     getCyPromptBundleStub = sinon.stub()
+    readFileStub = sinon.stub()
+    verifySignatureStub = sinon.stub()
+    pathExistsStub = sinon.stub()
 
     ensureCyPromptBundle = (proxyquire('../lib/cloud/cy-prompt/ensure_cy_prompt_bundle', {
       os: {
@@ -24,12 +34,17 @@ describe('ensureCyPromptBundle', () => {
       'fs-extra': {
         remove: rmStub.resolves(),
         ensureDir: ensureStub.resolves(),
+        readFile: readFileStub.resolves(JSON.stringify(mockManifest)),
+        pathExists: pathExistsStub.resolves(true),
       },
       tar: {
         extract: extractStub.resolves(),
       },
       '../api/cy-prompt/get_cy_prompt_bundle': {
-        getCyPromptBundle: getCyPromptBundleStub.resolves(),
+        getCyPromptBundle: getCyPromptBundleStub.resolves(mockResponseSignature),
+      },
+      '../encryption': {
+        verifySignature: verifySignatureStub.resolves(true),
       },
     })).ensureCyPromptBundle
   })
@@ -38,7 +53,7 @@ describe('ensureCyPromptBundle', () => {
     const cyPromptPath = path.join(os.tmpdir(), 'cypress', 'cy-prompt', '123')
     const bundlePath = path.join(cyPromptPath, 'bundle.tar')
 
-    await ensureCyPromptBundle({
+    const manifest = await ensureCyPromptBundle({
       cyPromptPath,
       cyPromptUrl: 'https://cypress.io/cy-prompt',
       projectId: '123',
@@ -46,6 +61,7 @@ describe('ensureCyPromptBundle', () => {
 
     expect(rmStub).to.be.calledWith(cyPromptPath)
     expect(ensureStub).to.be.calledWith(cyPromptPath)
+    expect(readFileStub).to.be.calledWith(path.join(cyPromptPath, 'manifest.json'), 'utf8')
     expect(getCyPromptBundleStub).to.be.calledWith({
       cyPromptUrl: 'https://cypress.io/cy-prompt',
       projectId: '123',
@@ -56,6 +72,34 @@ describe('ensureCyPromptBundle', () => {
       file: bundlePath,
       cwd: cyPromptPath,
     })
+
+    expect(verifySignatureStub).to.be.calledWith(JSON.stringify(mockManifest), mockResponseSignature)
+
+    expect(manifest).to.deep.eq(mockManifest)
+  })
+
+  it('should throw an error if the cy prompt bundle signature is invalid', async () => {
+    verifySignatureStub.resolves(false)
+
+    const ensureCyPromptBundlePromise = ensureCyPromptBundle({
+      cyPromptPath: '/tmp/cypress/cy-prompt/123',
+      cyPromptUrl: 'https://cypress.io/cy-prompt',
+      projectId: '123',
+    })
+
+    await expect(ensureCyPromptBundlePromise).to.be.rejectedWith('Unable to verify cy-prompt signature')
+  })
+
+  it('should throw an error if the cy prompt bundle manifest is not found', async () => {
+    pathExistsStub.resolves(false)
+
+    const ensureCyPromptBundlePromise = ensureCyPromptBundle({
+      cyPromptPath: '/tmp/cypress/cy-prompt/123',
+      cyPromptUrl: 'https://cypress.io/cy-prompt',
+      projectId: '123',
+    })
+
+    await expect(ensureCyPromptBundlePromise).to.be.rejectedWith('Unable to find cy-prompt manifest')
   })
 
   it('should throw an error if the cy prompt bundle download times out', async () => {
diff --git a/packages/types/src/cy-prompt/cy-prompt-server-types.ts b/packages/types/src/cy-prompt/cy-prompt-server-types.ts
index e2aeb7d752e..e9a4d4e22cc 100644
--- a/packages/types/src/cy-prompt/cy-prompt-server-types.ts
+++ b/packages/types/src/cy-prompt/cy-prompt-server-types.ts
@@ -8,6 +8,7 @@ import type ProtocolMapping from 'devtools-protocol/types/protocol-mapping.d'
 import type { Router } from 'express'
 import type { AxiosInstance } from 'axios'
 import type { Socket } from 'socket.io'
+import type { BinaryLike } from 'crypto'
 
 export type CyPromptCommands = ProtocolMapping.Commands
 
@@ -57,6 +58,8 @@ export interface CyPromptServerOptions {
   cyPromptPath: string
   projectSlug?: string
   cloudApi: CyPromptCloudApi
+  manifest: Record<string, string>
+  verifyHash: (contents: BinaryLike, expectedHash: string) => boolean
   getProjectOptions: () => Promise<CyPromptProjectOptions>
 }
 
diff --git a/scripts/after-pack-hook.js b/scripts/after-pack-hook.js
index ea0e365c283..562ba2904fc 100644
--- a/scripts/after-pack-hook.js
+++ b/scripts/after-pack-hook.js
@@ -19,6 +19,8 @@ const {
   getStudioFileSource,
   validateStudioFile,
   getIndexJscHash,
+  getCyPromptFileSource,
+  validateCyPromptFile,
   DUMMY_INDEX_JSC_HASH,
 } = require('./binary/binary-sources')
 const verify = require('../cli/lib/tasks/verify')
@@ -100,6 +102,12 @@ module.exports = async function (params) {
       const StudioLifecycleManagerPath = path.join(CY_ROOT_DIR, 'packages/server/lib/cloud/studio/StudioLifecycleManager.ts')
       const StudioLifecycleManagerFileSource = await getStudioFileSource(StudioLifecycleManagerPath)
 
+      // Remove local cy prompt env
+      const cyPromptLifecycleManagerPath = path.join(CY_ROOT_DIR, 'packages/server/lib/cloud/cy-prompt/CyPromptLifecycleManager.ts')
+      const cyPromptLifecycleManagerFileSource = await getCyPromptFileSource(cyPromptLifecycleManagerPath)
+      const cyPromptManagerPath = path.join(CY_ROOT_DIR, 'packages/server/lib/cloud/cy-prompt/CyPromptManager.ts')
+      const cyPromptManagerFileSource = await getCyPromptFileSource(cyPromptManagerPath)
+
       await Promise.all([
         fs.writeFile(encryptionFilePath, encryptionFileSource),
         fs.writeFile(cloudEnvironmentFilePath, cloudEnvironmentFileSource),
@@ -107,6 +115,8 @@ module.exports = async function (params) {
         fs.writeFile(cloudProtocolFilePath, cloudProtocolFileSource),
         fs.writeFile(reportStudioErrorPath, reportStudioErrorFileSource),
         fs.writeFile(StudioLifecycleManagerPath, StudioLifecycleManagerFileSource),
+        fs.writeFile(cyPromptLifecycleManagerPath, cyPromptLifecycleManagerFileSource),
+        fs.writeFile(cyPromptManagerPath, cyPromptManagerFileSource),
         fs.writeFile(path.join(outputFolder, 'index.js'), binaryEntryPointSource),
       ])
 
@@ -121,6 +131,8 @@ module.exports = async function (params) {
         validateProtocolFile(cloudProtocolFilePath),
         validateStudioFile(reportStudioErrorPath),
         validateStudioFile(StudioLifecycleManagerPath),
+        validateCyPromptFile(cyPromptLifecycleManagerPath),
+        validateCyPromptFile(cyPromptManagerPath),
       ])
 
       await flipFuses(
diff --git a/scripts/binary/binary-sources.js b/scripts/binary/binary-sources.js
index a6196eea094..11f1185956a 100644
--- a/scripts/binary/binary-sources.js
+++ b/scripts/binary/binary-sources.js
@@ -119,6 +119,16 @@ const getStudioFileSource = async (studioFilePath) => {
   return fileContents.replaceAll('process.env.CYPRESS_LOCAL_STUDIO_PATH', 'undefined')
 }
 
+const getCyPromptFileSource = async (cyPromptFilePath) => {
+  const fileContents = await fs.readFile(cyPromptFilePath, 'utf8')
+
+  if (!fileContents.includes('process.env.CYPRESS_LOCAL_CY_PROMPT_PATH')) {
+    throw new Error(`Expected to find CYPRESS_LOCAL_CY_PROMPT_PATH in cy prompt file`)
+  }
+
+  return fileContents.replaceAll('process.env.CYPRESS_LOCAL_CY_PROMPT_PATH', 'undefined')
+}
+
 const validateProtocolFile = async (protocolFilePath) => {
   const afterReplaceProtocol = await fs.readFile(protocolFilePath, 'utf8')
 
@@ -135,6 +145,14 @@ const validateStudioFile = async (studioFilePath) => {
   }
 }
 
+const validateCyPromptFile = async (cyPromptFilePath) => {
+  const afterReplaceCyPrompt = await fs.readFile(cyPromptFilePath, 'utf8')
+
+  if (afterReplaceCyPrompt.includes('process.env.CYPRESS_LOCAL_CY_PROMPT_PATH')) {
+    throw new Error(`Expected process.env.CYPRESS_LOCAL_CY_PROMPT_PATH to be stripped from cy prompt file`)
+  }
+}
+
 module.exports = {
   getBinaryEntryPointSource,
   getBinaryByteNodeEntryPointSource,
@@ -147,6 +165,8 @@ module.exports = {
   validateProtocolFile,
   getStudioFileSource,
   validateStudioFile,
+  getCyPromptFileSource,
+  validateCyPromptFile,
   getIndexJscHash,
   DUMMY_INDEX_JSC_HASH,
 }