diff --git a/deps/message-port/async-uv.cc b/deps/message-port/async-uv.cc
index 9a1b462e52..e12cf9f2c5 100644
--- a/deps/message-port/async-uv.cc
+++ b/deps/message-port/async-uv.cc
@@ -17,62 +17,149 @@
 #include "async-uv.h"
 #include <nd-logger.h>
 #include <uv.h>
-#include <functional>
 #include "debug-mem-trace.h"
 
-std::queue<AsyncUV::Task> AsyncUV::queue_;
-std::mutex AsyncUV::queue_mutex_;
+struct AsyncUV::LoopData {
+  uv_loop_t* loop{nullptr};
+  uv_async_t* handle{nullptr};
+  std::queue<Task> queue;
+  std::mutex queue_mutex;
+};
 
-AsyncUV::AsyncUV(uv_loop_t* loop, Task task) : uv_h_(nullptr), task_(task) {
-  if (loop && task) {
-    Init(loop, task);
-  }
+std::map<uv_loop_t*, AsyncUV::LoopData*> AsyncUV::loop_data_;
+std::mutex AsyncUV::loop_data_mutex_;
+std::queue<AsyncUV::Task> AsyncUV::pending_queue_;
+std::mutex AsyncUV::pending_queue_mutex_;
+
+AsyncUV::AsyncUV(uv_loop_t* loop, Task task) : loop_(loop), task_(task) {
   TRACE_ADD(ASYNC, this);
 }
 
 AsyncUV::~AsyncUV() {
-  if (!uv_h_) {
+  TRACE(ASYNC, "~AsyncUV");
+  TRACE_REMOVE(ASYNC, this);
+}
+
+void AsyncUV::OnAsyncCalled(uv_async_t* handle) {
+  auto* loop_data = static_cast<LoopData*>(handle->data);
+  if (loop_data == nullptr) {
     return;
   }
 
-  TRACE(ASYNC, "~AsyncUV");
-  TRACE_REMOVE(ASYNC, this);
+  std::queue<Task> tasks_to_run;
+  {
+    std::lock_guard<std::mutex> lock(loop_data->queue_mutex);
+    loop_data->queue.swap(tasks_to_run);
+  }
 
-  uv_close(reinterpret_cast<uv_handle_t*>(uv_h_), [](uv_handle_t* handle) {
-    TRACE(ASYNC, "~uv_close");
-    TRACE_REMOVE(ASYNC_UV, handle);
-    delete reinterpret_cast<uv_async_t*>(handle);
-  });
+  while (!tasks_to_run.empty()) {
+    Task& task = tasks_to_run.front();
+    if (task) {
+      TRACE(MSGPORT, "run task");
+      task(handle);
+      TRACE(MSGPORT, "/run task");
+    }
+    tasks_to_run.pop();
+  }
 }
 
-bool AsyncUV::Send(uv_loop_t* loop, Task task) {
+AsyncUV::LoopData* AsyncUV::GetLoopData(uv_loop_t* loop,
+                                        bool create_if_not_found) {
+  std::lock_guard<std::mutex> lock(loop_data_mutex_);
+  auto it = loop_data_.find(loop);
+  if (it != loop_data_.end()) {
+    return it->second;
+  }
+
+  if (!create_if_not_found || loop == nullptr) {
+    return nullptr;
+  }
+
+  auto* loop_data = new LoopData();
+  loop_data->loop = loop;
+  loop_data->handle = new uv_async_t();
+  loop_data->handle->data = loop_data;
+  uv_async_init(loop, loop_data->handle, OnAsyncCalled);
+  uv_unref(reinterpret_cast<uv_handle_t*>(loop_data->handle));
+  TRACE_ADD(ASYNC_UV, loop_data->handle);
+  loop_data_[loop] = loop_data;
+  return loop_data;
+}
+
+bool AsyncUV::InitPerThread(uv_loop_t* loop) {
   if (loop == nullptr) {
+    return false;
+  }
+
+  return GetLoopData(loop, true) != nullptr;
+}
+
+void AsyncUV::CleanupPerThread(uv_loop_t* loop) {
+  std::lock_guard<std::mutex> lock(loop_data_mutex_);
+  auto it = loop_data_.find(loop);
+  if (it == loop_data_.end()) {
+    return;
+  }
+
+  LoopData* loop_data = it->second;
+  loop_data_.erase(it);
+
+  if (!uv_is_closing(reinterpret_cast<uv_handle_t*>(loop_data->handle))) {
+    uv_close(reinterpret_cast<uv_handle_t*>(loop_data->handle),
+             [](uv_handle_t* handle) {
+               TRACE(ASYNC, "~uv_close");
+               TRACE_REMOVE(ASYNC_UV, handle);
+               auto* loop_data = static_cast<LoopData*>(handle->data);
+               delete loop_data->handle;
+               delete loop_data;
+             });
+  }
+}
+
+bool AsyncUV::Send(uv_loop_t* loop, Task task) {
+  if (loop == nullptr || !task) {
     TRACE(MSGPORT, "invalid loop");
     return false;
   }
-  return (new AsyncUV(loop, task))->Send();
+
+  LoopData* loop_data = GetLoopData(loop, true);
+  if (loop_data == nullptr) {
+    return false;
+  }
+
+  {
+    std::lock_guard<std::mutex> lock(loop_data->queue_mutex);
+    loop_data->queue.push(std::move(task));
+  }
+
+  uv_async_send(loop_data->handle);
+  return true;
 }
 
 size_t AsyncUV::EnqueueTask(Task task) {
   TRACE(MSGPORT, "EnqueueTask");
-  std::lock_guard<std::mutex> lock(queue_mutex_);
-  queue_.push(task);
-  return queue_.size();
+  std::lock_guard<std::mutex> lock(pending_queue_mutex_);
+  pending_queue_.push(std::move(task));
+  return pending_queue_.size();
 }
 
 bool AsyncUV::DrainPendingTasks(uv_loop_t* loop) {
-  TRACE(MSGPORT, "DrainPendingTasks");
-  std::lock_guard<std::mutex> lock(queue_mutex_);
-  TRACE(MSGPORT, "drain pending tasks %zu", queue_.size());
-
   if (loop == nullptr) {
     TRACE(MSGPORT, "invalid loop");
     return false;
   }
 
-  while (!queue_.empty()) {
-    AsyncUV::Send(loop, queue_.front());
-    queue_.pop();
+  TRACE(MSGPORT, "DrainPendingTasks");
+  std::queue<Task> pending_tasks;
+  {
+    std::lock_guard<std::mutex> lock(pending_queue_mutex_);
+    TRACE(MSGPORT, "drain pending tasks %zu", pending_queue_.size());
+    pending_queue_.swap(pending_tasks);
+  }
+
+  while (!pending_tasks.empty()) {
+    AsyncUV::Send(loop, std::move(pending_tasks.front()));
+    pending_tasks.pop();
   }
   TRACE(MSGPORT, "/drain pending tasks");
   return true;
@@ -80,41 +167,28 @@ bool AsyncUV::DrainPendingTasks(uv_loop_t* loop) {
 
 void AsyncUV::DeletePendingTasks() {
   TRACE(MSGPORT, "DeletePendingTasks");
-  std::lock_guard<std::mutex> lock(queue_mutex_);
-  TRACE(MSGPORT, "delete pending tasks %zu", queue_.size());
-  if (!queue_.empty()) {
+  std::lock_guard<std::mutex> lock(pending_queue_mutex_);
+  TRACE(MSGPORT, "delete pending tasks %zu", pending_queue_.size());
+  if (!pending_queue_.empty()) {
     std::queue<Task> empty;
-    std::swap(queue_, empty);
+    std::swap(pending_queue_, empty);
   }
 }
 
 bool AsyncUV::IsPendingTasksEmpty() {
   TRACE(MSGPORT, "IsPendingTasksEmpty");
-  std::lock_guard<std::mutex> lock(queue_mutex_);
-  return queue_.empty();
+  std::lock_guard<std::mutex> lock(pending_queue_mutex_);
+  return pending_queue_.empty();
 }
 
 void AsyncUV::Init(uv_loop_t* loop, Task task) {
+  loop_ = loop;
   task_ = task;
-
-  uv_h_ = new uv_async_t();
-  uv_h_->data = this;
-  uv_async_init(loop, uv_h_, [](uv_async_t* handle) {
-    auto event = static_cast<AsyncUV*>(handle->data);
-    if (event->task_) {
-      TRACE(MSGPORT, "run task");
-      event->task_(handle);
-      TRACE(MSGPORT, "/run task");
-    }
-    delete event;
-  });
-  TRACE_ADD(ASYNC_UV, uv_h_);
 }
 
 bool AsyncUV::Send() {
-  if (!uv_h_) {
+  if (loop_ == nullptr || !task_) {
     return false;
   }
-  uv_async_send(uv_h_);
-  return true;
+  return Send(loop_, std::move(task_));
 }
diff --git a/deps/message-port/async-uv.h b/deps/message-port/async-uv.h
index 1444b3189c..31858398c3 100644
--- a/deps/message-port/async-uv.h
+++ b/deps/message-port/async-uv.h
@@ -17,6 +17,7 @@
 #pragma once
 
 #include <functional>
+#include <map>
 #include <mutex>
 #include <queue>
 
@@ -26,6 +27,7 @@
 
 using uv_loop_t = struct uv_loop_s;
 using uv_async_t = struct uv_async_s;
+using uv_handle_t = struct uv_handle_s;
 
 class EXPORT_API AsyncUV {
  public:
@@ -39,6 +41,10 @@ class EXPORT_API AsyncUV {
   static void DeletePendingTasks();
   static bool IsPendingTasksEmpty();
 
+  // Register and cleanup one shared async handle per loop.
+  static bool InitPerThread(uv_loop_t* loop);
+  static void CleanupPerThread(uv_loop_t* loop);
+
   AsyncUV(uv_loop_t* loop = nullptr, Task task = nullptr);
   ~AsyncUV();
 
@@ -46,9 +52,15 @@ class EXPORT_API AsyncUV {
   bool Send();
 
  private:
-  uv_async_t* uv_h_;
+  struct LoopData;
+  static LoopData* GetLoopData(uv_loop_t* loop, bool create_if_not_found);
+  static void OnAsyncCalled(uv_async_t* handle);
+
+  uv_loop_t* loop_;
   Task task_;
 
-  static std::queue<Task> queue_;
-  static std::mutex queue_mutex_;
+  static std::map<uv_loop_t*, LoopData*> loop_data_;
+  static std::mutex loop_data_mutex_;
+  static std::queue<Task> pending_queue_;
+  static std::mutex pending_queue_mutex_;
 };
diff --git a/src/lwnode/nd-vm-main-message-port.cc b/src/lwnode/nd-vm-main-message-port.cc
index 1893d4c3d7..c52b3a2c62 100644
--- a/src/lwnode/nd-vm-main-message-port.cc
+++ b/src/lwnode/nd-vm-main-message-port.cc
@@ -38,6 +38,7 @@ MainMessagePort::MainMessagePort(std::shared_ptr<Port> port,
 MainMessagePort::~MainMessagePort() {
   LWNODE_DEV_FATAL_LOG("[MainMessagePort::~MainMessagePort]");
   Channel::DeletePendingMessages();
+  AsyncUV::CleanupPerThread(uv_loop_);
 }
 
 void MainMessagePort::SetMessageEventClass(FunctionObjectRef* klass) {
@@ -53,6 +54,12 @@ void MainMessagePort::Init(ContextRef* context, uv_loop_t* loop) {
 
   context_ = context;
   uv_loop_ = loop;
+  AsyncUV::InitPerThread(uv_loop_);
+
+  // Drain once before publishing the loop, then drain again after publication
+  // to reduce the window where another thread can enqueue into the pending
+  // queue based on a stale "loop not ready" observation.
+  Channel::DrainPendingMessages(uv_loop_);
 
   try {
     internal_->uv_promise_.set_value(uv_loop_);