diff --git a/src/hotspot/os/windows/attachListener_windows.cpp b/src/hotspot/os/windows/attachListener_windows.cpp
index 2cc9d192ce5..10873a652f4 100644
--- a/src/hotspot/os/windows/attachListener_windows.cpp
+++ b/src/hotspot/os/windows/attachListener_windows.cpp
@@ -64,6 +64,11 @@
 class PipeChannel : public AttachOperation::RequestReader, public AttachOperation::ReplyWriter {
 private:
   HANDLE _hPipe;
+  void close_impl() {
+    FlushFileBuffers(_hPipe);
+    CloseHandle(_hPipe);
+    _hPipe = INVALID_HANDLE_VALUE;
+  }
 public:
   PipeChannel() : _hPipe(INVALID_HANDLE_VALUE) {}
   ~PipeChannel() {
@@ -92,10 +97,14 @@ public:
 
   void close() {
     if (opened()) {
-      ThreadBlockInVM tbivm(JavaThread::current());
-      FlushFileBuffers(_hPipe);
-      CloseHandle(_hPipe);
-      _hPipe = INVALID_HANDLE_VALUE;
+      JavaThread* current = JavaThread::current();
+      // if we fail to read/parse request from Win32AttachListener::dequeue, current thread is already blocked
+      if (current->thread_state() == _thread_blocked) {
+        close_impl();
+      } else {
+        ThreadBlockInVM tbivm(current);
+        close_impl();
+      }
     }
   }
 
diff --git a/test/hotspot/jtreg/serviceability/attach/FailedDequeueTest.java b/test/hotspot/jtreg/serviceability/attach/FailedDequeueTest.java
new file mode 100644
index 00000000000..fd1f0c42c42
--- /dev/null
+++ b/test/hotspot/jtreg/serviceability/attach/FailedDequeueTest.java
@@ -0,0 +1,71 @@
+/*
+ * Copyright (c) 2025, Oracle and/or its affiliates. All rights reserved.
+ * DO NOT ALTER OR REMOVE COPYRIGHT NOTICES OR THIS FILE HEADER.
+ *
+ * This code is free software; you can redistribute it and/or modify it
+ * under the terms of the GNU General Public License version 2 only, as
+ * published by the Free Software Foundation.
+ *
+ * This code is distributed in the hope that it will be useful, but WITHOUT
+ * ANY WARRANTY; without even the implied warranty of MERCHANTABILITY or
+ * FITNESS FOR A PARTICULAR PURPOSE.  See the GNU General Public License
+ * version 2 for more details (a copy is included in the LICENSE file that
+ * accompanied this code).
+ *
+ * You should have received a copy of the GNU General Public License version
+ * 2 along with this work; if not, write to the Free Software Foundation,
+ * Inc., 51 Franklin St, Fifth Floor, Boston, MA 02110-1301 USA.
+ *
+ * Please contact Oracle, 500 Oracle Parkway, Redwood Shores, CA 94065 USA
+ * or visit www.oracle.com if you need additional information or have any
+ * questions.
+ */
+
+/*
+ * @test
+ * @summary verifies that failure in AttachListener::dequeue does not crash the VM
+ * @bug 8356177
+ * @library /test/lib
+ * @modules jdk.attach/sun.tools.attach
+ *
+ * @run driver FailedDequeueTest
+ */
+
+import java.io.IOException;
+
+import com.sun.tools.attach.VirtualMachine;
+import sun.tools.attach.HotSpotVirtualMachine;
+
+import jdk.test.lib.apps.LingeredApp;
+
+public class FailedDequeueTest {
+
+    public static void main(String[] args) throws Exception {
+        LingeredApp app = null;
+        try {
+            app = LingeredApp.startApp("-Xlog:attach=trace");
+            test(app);
+        } finally {
+            LingeredApp.stopApp(app);
+        }
+    }
+
+    // The test uses HotSpotVirtualMachine.setFlag method with long flag value (longer than 256K).
+    private static String flagName = "HeapDumpPath";
+    private static String flagValue = "X" + "A".repeat(256 * 1024) + "X";
+
+    private static void test(LingeredApp app) throws Exception {
+        HotSpotVirtualMachine vm = (HotSpotVirtualMachine)VirtualMachine.attach(String.valueOf(app.getPid()));
+        try {
+            // Should throw IOException and don't crash
+            vm.setFlag(flagName, flagValue);
+
+            throw new RuntimeException("expected IOException is not thrown");
+        } catch (IOException ex) {
+            System.out.println("OK: setFlag thrown expected exception:");
+            ex.printStackTrace(System.out);
+        } finally {
+            vm.detach();
+        }
+    }
+}