diff --git a/src/lib/functions/registry.mjs b/src/lib/functions/registry.mjs
index aea023fcdba..ff8e5772b7f 100644
--- a/src/lib/functions/registry.mjs
+++ b/src/lib/functions/registry.mjs
@@ -212,7 +212,10 @@ export class FunctionsRegistry {
     await Promise.all(deletedFunctions.map((func) => this.unregisterFunction(func.name)))
 
     await Promise.all(
-      functions.map(async ({ displayName, mainFile, name, runtime: runtimeName }) => {
+      // zip-it-and-ship-it returns an array sorted based on which extension should have precedence,
+      // where the last ones precede the previous ones. This is why
+      // we reverse the array so we get the right functions precedence in the CLI.
+      functions.reverse().map(async ({ displayName, mainFile, name, runtime: runtimeName }) => {
         const runtime = runtimes[runtimeName]
 
         // If there is no matching runtime, it means this function is not yet
diff --git a/src/lib/functions/server.mjs b/src/lib/functions/server.mjs
index c630a83a170..af43794e1d7 100644
--- a/src/lib/functions/server.mjs
+++ b/src/lib/functions/server.mjs
@@ -222,9 +222,9 @@ export const startFunctionsServer = async (options) => {
       functionsDirectories.push(distPath)
     }
   } else {
-    // The order of the function directories matters. Leftmost directories take
+    // The order of the function directories matters. Rightmost directories take
     // precedence.
-    const sourceDirectories = [settings.functions, internalFunctionsDir].filter(Boolean)
+    const sourceDirectories = [internalFunctionsDir, settings.functions].filter(Boolean)
 
     functionsDirectories.push(...sourceDirectories)
   }
diff --git a/tests/unit/lib/functions/registry.test.mjs b/tests/unit/lib/functions/registry.test.mjs
index 78b60167abe..2a44990d403 100644
--- a/tests/unit/lib/functions/registry.test.mjs
+++ b/tests/unit/lib/functions/registry.test.mjs
@@ -1,8 +1,40 @@
-import { expect, test, vi } from 'vitest'
+import { mkdir, mkdtemp, writeFile } from 'fs/promises'
+import { tmpdir } from 'os'
+import { join } from 'path'
+
+import { describe, expect, test, vi } from 'vitest'
 
 import { FunctionsRegistry } from '../../../../src/lib/functions/registry.mjs'
 import { watchDebounced } from '../../../../src/utils/command-helpers.mjs'
 
+const duplicateFunctions = [
+  {
+    filename: 'hello.js',
+    content: `exports.handler = async (event) => ({ statusCode: 200, body: JSON.stringify({ message: 'Hello World from .js' }) })`,
+  },
+  {
+    filename: 'hello.ts',
+    content: `exports.handler = async (event) => ({ statusCode: 200, body: JSON.stringify({ message: 'Hello World from .ts' }) })`,
+  },
+  {
+    filename: 'hello2.js',
+    content: `exports.handler = async (event) => ({ statusCode: 200, body: JSON.stringify({ message: 'Hello World from .ts' }) })`,
+  },
+  {
+    filename: 'hello2/main.go',
+    subDir: 'hello2',
+    content: `package main
+    import (
+      "fmt"
+    )
+
+    func main() {
+      fmt.Println("Hello, world from a go function!")
+    }
+    `,
+  },
+]
+
 vi.mock('../../../../src/utils/command-helpers.mjs', async () => {
   const helpers = await vi.importActual('../../../../src/utils/command-helpers.mjs')
 
@@ -35,6 +67,40 @@ test('registry should only pass functions config to zip-it-and-ship-it', async (
   await prepareDirectoryScanStub.mockRestore()
 })
 
+describe('the registry handles duplicate functions based on extension precedence', () => {
+  test('where .js takes precedence over .go, and .go over .ts', async () => {
+    const projectRoot = await mkdtemp(join(tmpdir(), 'functions-extension-precedence'))
+    const functionsDirectory = join(projectRoot, 'functions')
+    await mkdir(functionsDirectory)
+
+    duplicateFunctions.forEach(async (func) => {
+      if (func.subDir) {
+        const subDir = join(functionsDirectory, func.subDir)
+        await mkdir(subDir)
+      }
+      const file = join(functionsDirectory, func.filename)
+      await writeFile(file, func.content)
+    })
+    const functionsRegistry = new FunctionsRegistry({
+      projectRoot,
+      config: {},
+      timeouts: { syncFunctions: 1, backgroundFunctions: 1 },
+      settings: { port: 8888 },
+    })
+    const prepareDirectoryScanStub = vi.spyOn(FunctionsRegistry, 'prepareDirectoryScan').mockImplementation(() => {})
+    const setupDirectoryWatcherStub = vi.spyOn(functionsRegistry, 'setupDirectoryWatcher').mockImplementation(() => {})
+
+    await functionsRegistry.scan([functionsDirectory])
+    const { functions } = functionsRegistry
+
+    expect(functions.get('hello').runtime.name).toBe('js')
+    expect(functions.get('hello2').runtime.name).toBe('go')
+
+    await setupDirectoryWatcherStub.mockRestore()
+    await prepareDirectoryScanStub.mockRestore()
+  })
+})
+
 test('should add included_files to watcher', async () => {
   const registry = new FunctionsRegistry({})
   const func = {