diff --git a/src/env-inl.h b/src/env-inl.h
index 08fe98e10b7716..8fdcf293805429 100644
--- a/src/env-inl.h
+++ b/src/env-inl.h
@@ -235,12 +235,6 @@ inline uv_idle_t* Environment::immediate_idle_handle() {
   return &immediate_idle_handle_;
 }
 
-inline void Environment::RegisterHandleCleanup(uv_handle_t* handle,
-                                               HandleCleanupCb cb,
-                                               void* arg) {
-  handle_cleanup_queue_.push_back(HandleCleanup{handle, cb, arg});
-}
-
 template <typename T, typename OnCloseCallback>
 inline void Environment::CloseHandle(T* handle, OnCloseCallback callback) {
   handle_cleanup_waiting_++;
diff --git a/src/env.cc b/src/env.cc
index c7c34be24b62c1..cfd19a491d1c8e 100644
--- a/src/env.cc
+++ b/src/env.cc
@@ -1099,13 +1099,8 @@ void Environment::InitializeLibuv() {
     }
   }
 
-  // Register clean-up cb to be called to clean up the handles
-  // when the environment is freed, note that they are not cleaned in
-  // the one environment per process setup, but will be called in
-  // FreeEnvironment.
-  RegisterHandleCleanups();
-
   StartProfilerIdleNotifier();
+  env_handle_initialized_ = true;
 }
 
 void Environment::InitializeCompileCache() {
@@ -1183,27 +1178,27 @@ void Environment::ExitEnv(StopFlags::Flags flags) {
   });
 }
 
-void Environment::RegisterHandleCleanups() {
-  HandleCleanupCb close_and_finish = [](Environment* env, uv_handle_t* handle,
-                                        void* arg) {
-    handle->data = env;
+void Environment::ClosePerEnvHandles() {
+  // If LoadEnvironment and InitializeLibuv are not called, like when building
+  // snapshots, skip closing the per environment handles.
+  if (!env_handle_initialized_) {
+    return;
+  }
 
-    env->CloseHandle(handle, [](uv_handle_t* handle) {
+  auto close_and_finish = [&](uv_handle_t* handle) {
+    CloseHandle(handle, [](uv_handle_t* handle) {
 #ifdef DEBUG
       memset(handle, 0xab, uv_handle_size(handle->type));
 #endif
     });
   };
 
-  auto register_handle = [&](uv_handle_t* handle) {
-    RegisterHandleCleanup(handle, close_and_finish, nullptr);
-  };
-  register_handle(reinterpret_cast<uv_handle_t*>(timer_handle()));
-  register_handle(reinterpret_cast<uv_handle_t*>(immediate_check_handle()));
-  register_handle(reinterpret_cast<uv_handle_t*>(immediate_idle_handle()));
-  register_handle(reinterpret_cast<uv_handle_t*>(&idle_prepare_handle_));
-  register_handle(reinterpret_cast<uv_handle_t*>(&idle_check_handle_));
-  register_handle(reinterpret_cast<uv_handle_t*>(&task_queues_async_));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(timer_handle()));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(immediate_check_handle()));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(immediate_idle_handle()));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(&idle_prepare_handle_));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(&idle_check_handle_));
+  close_and_finish(reinterpret_cast<uv_handle_t*>(&task_queues_async_));
 }
 
 void Environment::CleanupHandles() {
@@ -1223,10 +1218,6 @@ void Environment::CleanupHandles() {
   for (HandleWrap* handle : handle_wrap_queue_)
     handle->Close();
 
-  for (HandleCleanup& hc : handle_cleanup_queue_)
-    hc.cb_(this, hc.handle_, hc.arg_);
-  handle_cleanup_queue_.clear();
-
   while (handle_cleanup_waiting_ != 0 ||
          request_waiting_ != 0 ||
          !handle_wrap_queue_.IsEmpty()) {
@@ -1280,6 +1271,7 @@ MaybeLocal<Value> Environment::RunSnapshotDeserializeMain() const {
 void Environment::RunCleanup() {
   started_cleanup_ = true;
   TRACE_EVENT0(TRACING_CATEGORY_NODE1(environment), "RunCleanup");
+  ClosePerEnvHandles();
   // Only BaseObject's cleanups are registered as per-realm cleanup hooks now.
   // Defer the BaseObject cleanup after handles are cleaned up.
   CleanupHandles();
diff --git a/src/env.h b/src/env.h
index c45249d49f0a58..118ccf16cdeed1 100644
--- a/src/env.h
+++ b/src/env.h
@@ -678,24 +678,10 @@ class Environment final : public MemoryRetainer {
   inline const std::vector<std::string>& argv();
   const std::string& exec_path() const;
 
-  typedef void (*HandleCleanupCb)(Environment* env,
-                                  uv_handle_t* handle,
-                                  void* arg);
-  struct HandleCleanup {
-    uv_handle_t* handle_;
-    HandleCleanupCb cb_;
-    void* arg_;
-  };
-
-  void RegisterHandleCleanups();
   void CleanupHandles();
   void Exit(ExitCode code);
   void ExitEnv(StopFlags::Flags flags);
-
-  // Register clean-up cb to be called on environment destruction.
-  inline void RegisterHandleCleanup(uv_handle_t* handle,
-                                    HandleCleanupCb cb,
-                                    void* arg);
+  void ClosePerEnvHandles();
 
   template <typename T, typename OnCloseCallback>
   inline void CloseHandle(T* handle, OnCloseCallback callback);
@@ -1100,6 +1086,8 @@ class Environment final : public MemoryRetainer {
   std::list<binding::DLib> loaded_addons_;
   v8::Isolate* const isolate_;
   IsolateData* const isolate_data_;
+
+  bool env_handle_initialized_ = false;
   uv_timer_t timer_handle_;
   uv_check_t immediate_check_handle_;
   uv_idle_t immediate_idle_handle_;
@@ -1212,7 +1200,6 @@ class Environment final : public MemoryRetainer {
   CleanableQueue cleanable_queue_;
   HandleWrapQueue handle_wrap_queue_;
   ReqWrapQueue req_wrap_queue_;
-  std::list<HandleCleanup> handle_cleanup_queue_;
   int handle_cleanup_waiting_ = 0;
   int request_waiting_ = 0;