diff --git a/src/lib/functions/registry.mjs b/src/lib/functions/registry.mjs
index c48aa6794fd..85a563b3f7a 100644
--- a/src/lib/functions/registry.mjs
+++ b/src/lib/functions/registry.mjs
@@ -1,5 +1,5 @@
 // @ts-check
-import { mkdir } from 'fs/promises'
+import { mkdir, stat } from 'fs/promises'
 import { createRequire } from 'module'
 import { basename, extname, isAbsolute, join, resolve } from 'path'
 import { env } from 'process'
@@ -39,6 +39,7 @@ export class FunctionsRegistry {
     debug = false,
     isConnected = false,
     logLambdaCompat,
+    manifest,
     projectRoot,
     settings,
     timeouts,
@@ -96,6 +97,14 @@ export class FunctionsRegistry {
      * @type {boolean}
      */
     this.logLambdaCompat = Boolean(logLambdaCompat)
+
+    /**
+     * Contents of a `manifest.json` file that can be looked up when dealing
+     * with built functions.
+     *
+     * @type {object}
+     */
+    this.manifest = manifest
   }
 
   checkTypesPackage() {
@@ -390,12 +399,30 @@ export class FunctionsRegistry {
         FunctionsRegistry.logEvent('extracted', { func })
       }
 
-      func.mainFile = join(unzippedDirectory, `${func.name}.js`)
+      // If there's a manifest file, look up the function in order to extract
+      // the build data.
+      const manifestEntry = (this.manifest?.functions || []).find((manifestFunc) => manifestFunc.name === func.name)
+
+      func.buildData = manifestEntry?.buildData || {}
+
+      // When we look at an unzipped function, we don't know whether it uses
+      // the legacy entry file format (i.e. `[function name].js`) or the new
+      // one (i.e. `___netlify-entry-point.mjs`). Let's look for the new one
+      // and use it if it exists, otherwise use the old one.
+      try {
+        const v2EntryPointPath = join(unzippedDirectory, '___netlify-entry-point.mjs')
+
+        await stat(v2EntryPointPath)
+
+        func.mainFile = v2EntryPointPath
+      } catch {
+        func.mainFile = join(unzippedDirectory, `${func.name}.js`)
+      }
+    } else {
+      this.buildFunctionAndWatchFiles(func, !isReload)
     }
 
     this.functions.set(name, func)
-
-    this.buildFunctionAndWatchFiles(func, !isReload)
   }
 
   /**
diff --git a/src/lib/functions/server.mjs b/src/lib/functions/server.mjs
index d39bee53397..d0eadf4762b 100644
--- a/src/lib/functions/server.mjs
+++ b/src/lib/functions/server.mjs
@@ -1,6 +1,7 @@
 // @ts-check
 import { Buffer } from 'buffer'
 import { promises as fs } from 'fs'
+import path from 'path'
 
 import express from 'express'
 import expressLogging from 'express-logging'
@@ -261,6 +262,7 @@ export const startFunctionsServer = async (options) => {
     options
   const internalFunctionsDir = await getInternalFunctionsDir({ base: site.root })
   const functionsDirectories = []
+  let manifest
 
   // If the `loadDistFunctions` parameter is sent, the functions server will
   // use the built functions created by zip-it-and-ship-it rather than building
@@ -270,6 +272,18 @@ export const startFunctionsServer = async (options) => {
 
     if (distPath) {
       functionsDirectories.push(distPath)
+
+      // When using built functions, read the manifest file so that we can
+      // extract metadata such as routes and API version.
+      try {
+        const manifestPath = path.join(distPath, 'manifest.json')
+        // eslint-disable-next-line unicorn/prefer-json-parse-buffer
+        const data = await fs.readFile(manifestPath, 'utf8')
+
+        manifest = JSON.parse(data)
+      } catch {
+        // no-op
+      }
     }
   } else {
     // The order of the function directories matters. Rightmost directories take
@@ -297,6 +311,7 @@ export const startFunctionsServer = async (options) => {
     debug,
     isConnected: Boolean(siteUrl),
     logLambdaCompat: isFeatureFlagEnabled('cli_log_lambda_compat', siteInfo),
+    manifest,
     // functions always need to be inside the packagePath if set inside a monorepo
     projectRoot: command.workingDir,
     settings,