diff --git a/lib/internal/fs/watchers.js b/lib/internal/fs/watchers.js
index 2dad214a729c9c..af54f8c16c8fd8 100644
--- a/lib/internal/fs/watchers.js
+++ b/lib/internal/fs/watchers.js
@@ -317,6 +317,8 @@ FSWatcher.prototype[kFSWatchStart] = function(filename,
                                  encoding);
   if (err) {
     if (!throwIfNoEntry && err === UV_ENOENT) {
+      // FSEventWrap::Start() already started closing the native handle.
+      this._handle = null;
       return;
     }
 
diff --git a/test/parallel/test-fs-watch-enoent.js b/test/parallel/test-fs-watch-enoent.js
index e363b3e9325c8c..2120485a4e6cde 100644
--- a/test/parallel/test-fs-watch-enoent.js
+++ b/test/parallel/test-fs-watch-enoent.js
@@ -62,7 +62,11 @@ tmpdir.refresh();
     );
   } else {
     const watcher = fs.watch(nonexistentFile, { throwIfNoEntry: false }, common.mustNotCall());
-    watcher.close();
+    if (common.isLinux) {
+      setTimeout(common.mustCall(() => watcher.close()), common.platformTimeout(10));
+    } else {
+      watcher.close();
+    }
   }
 }
 
diff --git a/test/parallel/test-watch-mode-missing-env-file-signal.mjs b/test/parallel/test-watch-mode-missing-env-file-signal.mjs
new file mode 100644
index 00000000000000..502cc2ddc334b9
--- /dev/null
+++ b/test/parallel/test-watch-mode-missing-env-file-signal.mjs
@@ -0,0 +1,91 @@
+import * as common from '../common/index.mjs';
+import assert from 'node:assert';
+import { spawn } from 'node:child_process';
+import { once } from 'node:events';
+import { writeFileSync } from 'node:fs';
+import { clearTimeout, setTimeout } from 'node:timers';
+import tmpdir from '../common/tmpdir.js';
+
+if (!common.isLinux)
+  common.skip('This test verifies Linux fs.watch() behavior');
+
+tmpdir.refresh();
+const entry = tmpdir.resolve('entry.js');
+const missingEnvFile = tmpdir.resolve('missing.env');
+writeFileSync(entry, '');
+
+async function withTimeout(promise, message) {
+  let timeout;
+  const timedOut = new Promise((_, reject) => {
+    timeout = setTimeout(
+      () => reject(new Error(message)),
+      common.platformTimeout(10_000),
+    );
+  });
+
+  try {
+    return await Promise.race([promise, timedOut]);
+  } finally {
+    clearTimeout(timeout);
+  }
+}
+
+async function testSignal(signal) {
+  const child = spawn(process.execPath, [
+    '--watch',
+    `--env-file-if-exists=${missingEnvFile}`,
+    entry,
+  ], {
+    cwd: tmpdir.path,
+    stdio: ['ignore', 'pipe', 'pipe'],
+  });
+  const closed = once(child, 'close');
+  const ready = Promise.withResolvers();
+  let stdout = '';
+  let stderr = '';
+
+  child.stdout.setEncoding('utf8');
+  child.stdout.on('data', (data) => {
+    stdout += data;
+    if (stdout.includes('Completed running')) {
+      ready.resolve();
+    }
+  });
+  child.stderr.setEncoding('utf8');
+  child.stderr.on('data', (data) => {
+    stderr += data;
+  });
+  child.once('error', ready.reject);
+  child.once('exit', (code, exitSignal) => {
+    ready.reject(new Error(
+      `Watch mode exited before becoming ready: code=${code}, signal=${exitSignal}`,
+    ));
+  });
+
+  try {
+    await withTimeout(
+      ready.promise,
+      'Timed out waiting for watch mode readiness',
+    );
+    assert.strictEqual(child.kill(signal), true);
+    const [code, exitSignal] = await withTimeout(
+      closed,
+      `Timed out waiting for watch mode to exit after ${signal}`,
+    );
+
+    assert.strictEqual(code, 0);
+    assert.strictEqual(exitSignal, null);
+    assert.doesNotMatch(
+      `${stdout}\n${stderr}`,
+      /Assertion failed|FSEventWrap::GetInitialized/,
+    );
+  } finally {
+    if (child.exitCode === null && child.signalCode === null) {
+      child.kill('SIGKILL');
+    }
+    await closed.catch(() => {});
+  }
+}
+
+await testSignal('SIGINT');
+await testSignal('SIGTERM');