diff --git a/lib/internal/fs/promises.js b/lib/internal/fs/promises.js
index 720bd1319b381f..2dfe9d8b518df6 100644
--- a/lib/internal/fs/promises.js
+++ b/lib/internal/fs/promises.js
@@ -107,7 +107,11 @@ const EventEmitter = require('events');
 const { StringDecoder } = require('string_decoder');
 const { kFSWatchStart, watch } = require('internal/fs/watchers');
 const nonNativeWatcher = require('internal/fs/recursive_watch');
-const { isIterable } = require('internal/streams/utils');
+const {
+  isIterable,
+  isReadableErrored,
+  isReadableNodeStream,
+} = require('internal/streams/utils');
 const assert = require('internal/assert');
 
 const permission = require('internal/process/permission');
@@ -1116,24 +1120,60 @@ function checkAborted(signal) {
     throw new AbortError(undefined, { cause: signal.reason });
 }
 
-async function writeFileHandle(filehandle, data, signal, encoding) {
-  checkAborted(signal);
+function makeWriteFileStreamErrorHandler(data) {
+  if (!isReadableNodeStream(data))
+    return undefined;
+
+  let error;
+  let errored = false;
+  function onError(err) {
+    error = err;
+    errored = true;
+  }
+  const streamError = isReadableErrored(data);
+  if (streamError != null)
+    onError(streamError);
+  data.on('error', onError);
+
+  return {
+    __proto__: null,
+    check() {
+      if (errored)
+        throw error;
+    },
+    cleanup() {
+      data.removeListener('error', onError);
+    },
+  };
+}
+
+async function writeFileHandle(filehandle, data, signal, encoding, streamErrorHandler) {
   if (isCustomIterable(data)) {
-    for await (const buf of data) {
+    streamErrorHandler ??= makeWriteFileStreamErrorHandler(data);
+    try {
       checkAborted(signal);
-      const toWrite =
-        isArrayBufferView(buf) ? buf : Buffer.from(buf, encoding || 'utf8');
-      let remaining = toWrite.byteLength;
-      while (remaining > 0) {
-        const writeSize = MathMin(kWriteFileMaxChunkSize, remaining);
-        const { bytesWritten } = await write(
-          filehandle, toWrite, toWrite.byteLength - remaining, writeSize);
-        remaining -= bytesWritten;
+      streamErrorHandler?.check();
+      for await (const buf of data) {
         checkAborted(signal);
+        streamErrorHandler?.check();
+        const toWrite =
+          isArrayBufferView(buf) ? buf : Buffer.from(buf, encoding || 'utf8');
+        let remaining = toWrite.byteLength;
+        while (remaining > 0) {
+          const writeSize = MathMin(kWriteFileMaxChunkSize, remaining);
+          const { bytesWritten } = await write(
+            filehandle, toWrite, toWrite.byteLength - remaining, writeSize);
+          remaining -= bytesWritten;
+          checkAborted(signal);
+          streamErrorHandler?.check();
+        }
       }
+    } finally {
+      streamErrorHandler?.cleanup();
     }
     return;
   }
+  checkAborted(signal);
   data = new Uint8Array(data.buffer, data.byteOffset, data.byteLength);
   let remaining = data.byteLength;
   if (remaining === 0) return;
@@ -1891,13 +1931,23 @@ async function writeFile(path, data, options) {
   }
 
   validateAbortSignal(options.signal);
+  checkAborted(options.signal);
+  const streamErrorHandler = makeWriteFileStreamErrorHandler(data);
+
   if (path instanceof FileHandle)
-    return writeFileHandle(path, data, options.signal, options.encoding);
+    return writeFileHandle(
+      path, data, options.signal, options.encoding, streamErrorHandler);
 
-  checkAborted(options.signal);
+  let fd;
+  try {
+    fd = await open(path, flag, options.mode);
+  } catch (err) {
+    streamErrorHandler?.cleanup();
+    throw err;
+  }
 
-  const fd = await open(path, flag, options.mode);
-  let writeOp = writeFileHandle(fd, data, options.signal, options.encoding);
+  let writeOp = writeFileHandle(
+    fd, data, options.signal, options.encoding, streamErrorHandler);
 
   if (flush) {
     writeOp = handleFdSync(writeOp, fd);
diff --git a/test/parallel/test-fs-promises-file-handle-writeFile.js b/test/parallel/test-fs-promises-file-handle-writeFile.js
index 2c1a80e4f52d49..7635ec57567db0 100644
--- a/test/parallel/test-fs-promises-file-handle-writeFile.js
+++ b/test/parallel/test-fs-promises-file-handle-writeFile.js
@@ -48,6 +48,7 @@ async function doWriteAndCancel() {
 
 const dest = path.resolve(tmpDir, 'tmp.txt');
 const otherDest = path.resolve(tmpDir, 'tmp-2.txt');
+const errorDest = path.resolve(tmpDir, 'tmp-error.txt');
 const stream = Readable.from(['a', 'b', 'c']);
 const stream2 = Readable.from(['ümlaut', ' ', 'sechzig']);
 const iterable = {
@@ -65,6 +66,15 @@ function iterableWith(value) {
     }
   };
 }
+
+function createEarlyErrorStream(error) {
+  const stream = new Readable({
+    read() {}
+  });
+  process.nextTick(() => stream.destroy(error));
+  return stream;
+}
+
 const bufferIterable = {
   expected: 'abc',
   *[Symbol.iterator]() {
@@ -94,6 +104,25 @@ async function doWriteStream() {
   }
 }
 
+async function doWriteStreamError() {
+  const fileHandle = await open(errorDest, 'w+');
+  const error = new Error('early file handle writeFile stream error');
+  const stream = createEarlyErrorStream(error);
+  const uncaughtException = common.mustNotCall(
+    'stream errors should reject FileHandle.writeFile()');
+
+  process.once('uncaughtException', uncaughtException);
+  try {
+    await assert.rejects(
+      fileHandle.writeFile(stream),
+      { message: error.message }
+    );
+  } finally {
+    process.removeListener('uncaughtException', uncaughtException);
+    await fileHandle.close();
+  }
+}
+
 async function doWriteStreamWithCancel() {
   const controller = new AbortController();
   const { signal } = controller;
@@ -190,6 +219,7 @@ async function doWriteInvalidValues() {
   await validateWriteFile();
   await doWriteAndCancel();
   await doWriteStream();
+  await doWriteStreamError();
   await doWriteStreamWithCancel();
   await doWriteIterable();
   await doWriteInvalidIterable();
diff --git a/test/parallel/test-fs-promises-writefile.js b/test/parallel/test-fs-promises-writefile.js
index 25df61b2b48414..4e90de47352d2b 100644
--- a/test/parallel/test-fs-promises-writefile.js
+++ b/test/parallel/test-fs-promises-writefile.js
@@ -13,6 +13,7 @@ tmpdir.refresh();
 
 const dest = path.resolve(tmpDir, 'tmp.txt');
 const otherDest = path.resolve(tmpDir, 'tmp-2.txt');
+const errorDest = path.resolve(tmpDir, 'tmp-error.txt');
 const buffer = Buffer.from('abc'.repeat(1000));
 const buffer2 = Buffer.from('xyz'.repeat(1000));
 const stream = Readable.from(['a', 'b', 'c']);
@@ -40,6 +41,15 @@ function iterableWith(value) {
     }
   };
 }
+
+function createEarlyErrorStream(error) {
+  const stream = new Readable({
+    read() {}
+  });
+  process.nextTick(() => stream.destroy(error));
+  return stream;
+}
+
 const bufferIterable = {
   expected: 'abc',
   *[Symbol.iterator]() {
@@ -70,6 +80,34 @@ async function doWriteStream() {
   assert.deepStrictEqual(data, expected);
 }
 
+async function doWriteStreamError() {
+  const error = new Error('early writeFile stream error');
+  const stream = createEarlyErrorStream(error);
+  const uncaughtException = common.mustNotCall(
+    'stream errors should reject writeFile()');
+
+  process.once('uncaughtException', uncaughtException);
+  try {
+    await assert.rejects(
+      fsPromises.writeFile(errorDest, stream),
+      { message: error.message }
+    );
+    assert.strictEqual(stream.listenerCount('error'), 0);
+  } finally {
+    process.removeListener('uncaughtException', uncaughtException);
+  }
+}
+
+async function doWriteStreamOpenError() {
+  const stream = Readable.from(['a']);
+
+  await assert.rejects(
+    fsPromises.writeFile(path.resolve(tmpDir, 'not-found', 'tmp.txt'), stream),
+    { code: 'ENOENT' }
+  );
+  assert.strictEqual(stream.listenerCount('error'), 0);
+}
+
 async function doWriteStreamWithCancel() {
   const controller = new AbortController();
   const { signal } = controller;
@@ -168,6 +206,8 @@ async function doReadWithEncoding() {
   await doRead();
   await doReadWithEncoding();
   await doWriteStream();
+  await doWriteStreamError();
+  await doWriteStreamOpenError();
   await doWriteStreamWithCancel();
   await doWriteIterable();
   await doWriteInvalidIterable();