diff --git a/packages/app/src/cli/services/function/build.test.ts b/packages/app/src/cli/services/function/build.test.ts
index b1ca9f3f7e..677900c336 100644
--- a/packages/app/src/cli/services/function/build.test.ts
+++ b/packages/app/src/cli/services/function/build.test.ts
@@ -4,7 +4,7 @@ import {testApp, testFunctionExtension} from '../../models/app/app.test-data.js'
 import {beforeEach, describe, expect, test, vi} from 'vitest'
 import {exec} from '@shopify/cli-kit/node/system'
 import {joinPath} from '@shopify/cli-kit/node/path'
-import {inTemporaryDirectory, mkdir, writeFile} from '@shopify/cli-kit/node/fs'
+import {inTemporaryDirectory, mkdir, writeFile, removeFile} from '@shopify/cli-kit/node/fs'
 import {build as esBuild} from 'esbuild'
 
 vi.mock('@shopify/cli-kit/node/system')
@@ -63,6 +63,10 @@ async function installShopifyLibrary(tmpDir: string) {
   const shopifyFunction = joinPath(shopifyFunctionDir, 'index.ts')
   await mkdir(shopifyFunctionDir)
   await writeFile(shopifyFunction, '')
+
+  const runModule = joinPath(shopifyFunctionDir, 'run.ts')
+  await writeFile(runModule, '')
+
   return shopifyFunction
 }
 
@@ -112,7 +116,23 @@ describe('bundleExtension', () => {
       const got = bundleExtension(ourFunction, {stdout, stderr, signal, app})
 
       // Then
-      await expect(got).rejects.toThrow(/Could not find the Shopify Function runtime/)
+      await expect(got).rejects.toThrow(/Could not find the Shopify Functions JavaScript library/)
+    })
+  })
+
+  test('errors if shopify library lacks the run module', async () => {
+    await inTemporaryDirectory(async (tmpDir) => {
+      // Given
+      const ourFunction = await testFunctionExtension({dir: tmpDir})
+      ourFunction.entrySourceFilePath = joinPath(tmpDir, 'src/index.ts')
+      const shopifyFunction = await installShopifyLibrary(tmpDir)
+      await removeFile(joinPath(shopifyFunction, '..', 'run.ts'))
+
+      // When
+      const got = bundleExtension(ourFunction, {stdout, stderr, signal, app})
+
+      // Then
+      await expect(got).rejects.toThrow(/Could not find the Shopify Functions JavaScript library/)
     })
   })
 
@@ -173,6 +193,7 @@ describe('ExportJavyBuilder', () => {
         // Given
         const ourFunction = await testFunctionExtension({dir: tmpDir})
         ourFunction.entrySourceFilePath = joinPath(tmpDir, 'src/index.ts')
+        const shopifyFunction = await installShopifyLibrary(tmpDir)
 
         // When
         const got = builder.bundle(
@@ -210,6 +231,7 @@ describe('ExportJavyBuilder', () => {
       await inTemporaryDirectory(async (tmpDir) => {
         // Given
         const ourFunction = await testFunctionExtension({dir: tmpDir})
+        const shopifyFunction = await installShopifyLibrary(tmpDir)
 
         // When
         const got = builder.bundle(ourFunction, {stdout, stderr, signal, app})
diff --git a/packages/app/src/cli/services/function/build.ts b/packages/app/src/cli/services/function/build.ts
index 4990f85393..ed35eb1aa1 100644
--- a/packages/app/src/cli/services/function/build.ts
+++ b/packages/app/src/cli/services/function/build.ts
@@ -5,7 +5,7 @@ import {FunctionConfigType} from '../../models/extensions/specifications/functio
 import {AppInterface} from '../../models/app/app.js'
 import {EsbuildEnvVarRegex} from '../../constants.js'
 import {hyphenate, camelize} from '@shopify/cli-kit/common/string'
-import {outputDebug} from '@shopify/cli-kit/node/output'
+import {outputContent, outputDebug, outputToken} from '@shopify/cli-kit/node/output'
 import {exec} from '@shopify/cli-kit/node/system'
 import {joinPath} from '@shopify/cli-kit/node/path'
 import {build as esBuild, BuildResult} from 'esbuild'
@@ -14,6 +14,7 @@ import {AbortSignal} from '@shopify/cli-kit/node/abort'
 import {renderTasks} from '@shopify/cli-kit/node/ui'
 import {pickBy} from '@shopify/cli-kit/common/object'
 import {runWithTimer} from '@shopify/cli-kit/node/metadata'
+import {AbortError} from '@shopify/cli-kit/node/error'
 import {Writable} from 'stream'
 
 interface JSFunctionBuildOptions {
@@ -104,24 +105,47 @@ export async function buildGraphqlTypes(
   })
 }
 
-export async function bundleExtension(
-  fun: ExtensionInstance<FunctionConfigType>,
-  options: JSFunctionBuildOptions,
-  processEnv = process.env,
-) {
+async function checkForShopifyFunctionRuntimeEntrypoint(fun: ExtensionInstance<FunctionConfigType>) {
   const entryPoint = await findPathUp('node_modules/@shopify/shopify_function/index.ts', {
     type: 'file',
     cwd: fun.directory,
   })
-  if (!entryPoint) {
-    throw new Error(
-      "Could not find the Shopify Function runtime. Make sure you have '@shopify/shopify_function' installed",
+
+  const runModule = await findPathUp('node_modules/@shopify/shopify_function/run.ts', {
+    type: 'file',
+    cwd: fun.directory,
+  })
+
+  if (!entryPoint || !runModule) {
+    throw new AbortError(
+      'Could not find the Shopify Functions JavaScript library.',
+      outputContent`Make sure you have the latest ${outputToken.yellow(
+        '@shopify/shopify_function',
+      )} library installed.`,
+      [
+        outputContent`Add ${outputToken.green(
+          '"@shopify/shopify_function": "1.0.0"',
+        )} to the dependencies section of the package.json file in your function's directory, if not already present.`
+          .value,
+        `Run your package manager's install command to update dependencies.`,
+      ],
     )
   }
+
   if (!fun.entrySourceFilePath) {
-    throw new Error('Could not find your function entry point. It must be in src/index.js or src/index.ts')
+    throw new AbortError('Could not find your function entry point. It must be in src/index.js or src/index.ts')
   }
 
+  return entryPoint
+}
+
+export async function bundleExtension(
+  fun: ExtensionInstance<FunctionConfigType>,
+  options: JSFunctionBuildOptions,
+  processEnv = process.env,
+) {
+  const entryPoint = await checkForShopifyFunctionRuntimeEntrypoint(fun)
+
   const esbuildOptions = {
     ...getESBuildOptions(fun.directory, fun.entrySourceFilePath, options.app.dotenv?.variables ?? {}, processEnv),
     entryPoints: [entryPoint],
@@ -227,9 +251,7 @@ export class ExportJavyBuilder implements JavyBuilder {
   }
 
   async bundle(fun: ExtensionInstance<FunctionConfigType>, options: JSFunctionBuildOptions, processEnv = process.env) {
-    if (!fun.entrySourceFilePath) {
-      throw new Error('Could not find your function entry point. It must be in src/index.js or src/index.ts')
-    }
+    await checkForShopifyFunctionRuntimeEntrypoint(fun)
 
     const contents = this.entrypointContents
     outputDebug('Generating dist/function.js using generated module:')