diff --git a/lib/internal/fs/promises.js b/lib/internal/fs/promises.js
index 8966a576ea8cd0..5184a28d326f3e 100644
--- a/lib/internal/fs/promises.js
+++ b/lib/internal/fs/promises.js
@@ -111,6 +111,7 @@ const kHandle = Symbol('kHandle');
 const kFd = Symbol('kFd');
 const kRefs = Symbol('kRefs');
 const kClosePromise = Symbol('kClosePromise');
+const kCloseReason = Symbol('kCloseReason');
 const kCloseResolve = Symbol('kCloseResolve');
 const kCloseReject = Symbol('kCloseReject');
 const kRef = Symbol('kRef');
@@ -389,6 +390,7 @@ class FileHandle extends EventEmitter {
 
     const handle = this[kHandle];
     this[kFd] = -1;
+    this[kCloseReason] = 'The FileHandle has been transferred';
     this[kHandle] = null;
     this[kRefs] = 0;
 
@@ -455,7 +457,7 @@ async function fsCall(fn, handle, ...args) {
 
   if (handle.fd === -1) {
     // eslint-disable-next-line no-restricted-syntax
-    const err = new Error('file closed');
+    const err = new Error(handle[kCloseReason] ?? 'file closed');
     err.code = 'EBADF';
     err.syscall = fn.name;
     throw err;
diff --git a/test/parallel/test-worker-message-port-transfer-filehandle.js b/test/parallel/test-worker-message-port-transfer-filehandle.js
index 3e6afe22a8c636..6052170c69f6e1 100644
--- a/test/parallel/test-worker-message-port-transfer-filehandle.js
+++ b/test/parallel/test-worker-message-port-transfer-filehandle.js
@@ -69,6 +69,11 @@ const { once } = require('events');
   assert.strictEqual(fh.fd, -1);
 
   port1.postMessage('second message');
+  await assert.rejects(() => fh.read(), {
+    code: 'EBADF',
+    message: 'The FileHandle has been transferred',
+    syscall: 'read'
+  });
 })().then(common.mustCall());
 
 (async function() {