diff --git a/packages/cli/src/util/dev/server.ts b/packages/cli/src/util/dev/server.ts
index 3a66340b3..fb5ce4ea0 100644
--- a/packages/cli/src/util/dev/server.ts
+++ b/packages/cli/src/util/dev/server.ts
@@ -329,6 +329,8 @@ export default class DevServer {
   ): Promise<void> {
     const name = relative(this.cwd, fsPath);
     try {
+      await this.getVercelConfig();
+
       this.files[name] = await FileFsRef.fromFsPath({ fsPath });
       const extensionless = this.getExtensionlessFile(name);
       if (extensionless) {
diff --git a/packages/cli/test/dev/fixtures/no-api/vercel.json b/packages/cli/test/dev/fixtures/no-api/vercel.json
new file mode 100644
index 000000000..85deee8e2
--- /dev/null
+++ b/packages/cli/test/dev/fixtures/no-api/vercel.json
@@ -0,0 +1,3 @@
+{
+  "version": 2
+}
diff --git a/packages/cli/test/dev/integration-2.test.ts b/packages/cli/test/dev/integration-2.test.ts
index 0d5e1bc50..9e3380f92 100644
--- a/packages/cli/test/dev/integration-2.test.ts
+++ b/packages/cli/test/dev/integration-2.test.ts
@@ -1,7 +1,17 @@
 // eslint-disable-next-line
-import path from 'path';
+import { join } from 'path';
+import ms from 'ms';
+import fs, { mkdirp } from 'fs-extra';
 
-const { exec, fixture, testFixture, testFixtureStdio } = require('./utils.js');
+const {
+  exec,
+  fetch,
+  fixture,
+  sleep,
+  testFixture,
+  testFixtureStdio,
+  validateResponseHeaders,
+} = require('./utils.js');
 
 test('[vercel dev] validate redirects', async () => {
   const directory = fixture('invalid-redirects');
@@ -334,3 +344,44 @@ test(
     await testPath(200, '/', /A simple deployment with the Vercel API!/m);
   })
 );
+
+test(
+  '[vercel dev] add a `api/fn.ts` when `api` does not exist at startup`',
+  testFixtureStdio('no-api', async (_testPath: any, port: any) => {
+    const directory = fixture('no-api');
+    const apiDir = join(directory, 'api');
+
+    try {
+      {
+        const response = await fetch(`http://localhost:${port}/api/new-file`);
+        validateResponseHeaders(response);
+        expect(response.status).toBe(404);
+      }
+
+      const fileContents = `
+          export const config = {
+            runtime: 'experimental-edge'
+          }
+
+          export default async function edge(request, event) {
+            return new Response('from new file');
+          }
+        `;
+
+      await mkdirp(apiDir);
+      await fs.writeFile(join(apiDir, 'new-file.js'), fileContents);
+
+      // Wait until file events have been processed
+      await sleep(ms('1s'));
+
+      {
+        const response = await fetch(`http://localhost:${port}/api/new-file`);
+        validateResponseHeaders(response);
+        const body = await response.text();
+        expect(body.trim()).toBe('from new file');
+      }
+    } finally {
+      await fs.remove(apiDir);
+    }
+  })
+);