Index: lldb/include/lldb/Core/Debugger.h
===================================================================
--- lldb/include/lldb/Core/Debugger.h
+++ lldb/include/lldb/Core/Debugger.h
@@ -191,13 +191,11 @@
                                        lldb::StreamFileSP &err);
 
   void PushIOHandler(const lldb::IOHandlerSP &reader_sp,
-                     bool cancel_top_handler = true);
+                     bool cancel_top_handler = true,
+                     bool asynchronous_if_needed = false);
 
   bool PopIOHandler(const lldb::IOHandlerSP &reader_sp);
 
-  // Synchronously run an input reader until it is done
-  void RunIOHandler(const lldb::IOHandlerSP &reader_sp);
-
   bool IsTopIOHandler(const lldb::IOHandlerSP &reader_sp);
 
   bool CheckTopIOHandlerTypes(IOHandler::Type top_type,
@@ -403,6 +401,9 @@
       m_script_interpreters;
 
   IOHandlerStack m_input_reader_stack;
+  std::mutex m_synchronous_reader_mutex;
+  std::unique_lock<std::mutex> m_synchronous_reader_lock;
+
   llvm::StringMap<std::weak_ptr<llvm::raw_ostream>> m_log_streams;
   std::shared_ptr<llvm::raw_ostream> m_log_callback_stream_sp;
   ConstString m_instance_name;
Index: lldb/source/Core/Debugger.cpp
===================================================================
--- lldb/source/Core/Debugger.cpp
+++ lldb/source/Core/Debugger.cpp
@@ -708,9 +708,10 @@
       m_source_manager_up(), m_source_file_cache(),
       m_command_interpreter_up(
           std::make_unique<CommandInterpreter>(*this, false)),
-      m_input_reader_stack(), m_instance_name(), m_loaded_plugins(),
-      m_event_handler_thread(), m_io_handler_thread(),
-      m_sync_broadcaster(nullptr, "lldb.debugger.sync"),
+      m_input_reader_stack(),
+      m_synchronous_reader_lock(m_synchronous_reader_mutex, std::defer_lock),
+      m_instance_name(), m_loaded_plugins(), m_event_handler_thread(),
+      m_io_handler_thread(), m_sync_broadcaster(nullptr, "lldb.debugger.sync"),
       m_forward_listener_sp(), m_clear_once() {
   char instance_cstr[256];
   snprintf(instance_cstr, sizeof(instance_cstr), "debugger_%d", (int)GetID());
@@ -895,6 +896,11 @@
 }
 
 void Debugger::ExecuteIOHandlers() {
+  // Prevent anyone from executing the IO handlers synchronously while they're
+  // running here.
+  std::lock_guard<std::unique_lock<std::mutex>> guard(
+      m_synchronous_reader_lock);
+
   while (true) {
     IOHandlerSP reader_sp(m_input_reader_stack.Top());
     if (!reader_sp)
@@ -941,28 +947,6 @@
   return m_input_reader_stack.GetTopIOHandlerHelpPrologue();
 }
 
-void Debugger::RunIOHandler(const IOHandlerSP &reader_sp) {
-  PushIOHandler(reader_sp);
-
-  IOHandlerSP top_reader_sp = reader_sp;
-  while (top_reader_sp) {
-    top_reader_sp->Run();
-
-    if (top_reader_sp.get() == reader_sp.get()) {
-      if (PopIOHandler(reader_sp))
-        break;
-    }
-
-    while (true) {
-      top_reader_sp = m_input_reader_stack.Top();
-      if (top_reader_sp && top_reader_sp->GetIsDone())
-        PopIOHandler(top_reader_sp);
-      else
-        break;
-    }
-  }
-}
-
 void Debugger::AdoptTopIOHandlerFilesIfInvalid(FileSP &in, StreamFileSP &out,
                                                StreamFileSP &err) {
   // Before an IOHandler runs, it must have in/out/err streams. This function
@@ -1005,7 +989,8 @@
 }
 
 void Debugger::PushIOHandler(const IOHandlerSP &reader_sp,
-                             bool cancel_top_handler) {
+                             bool cancel_top_handler,
+                             bool asynchronous_if_needed) {
   if (!reader_sp)
     return;
 
@@ -1029,6 +1014,12 @@
     if (cancel_top_handler)
       top_reader_sp->Cancel();
   }
+
+  // Support running the IO handlers synchronously on the current thread if
+  // they aren't running yet.
+  if (asynchronous_if_needed && !m_synchronous_reader_lock.owns_lock()) {
+    ExecuteIOHandlers();
+  }
 }
 
 bool Debugger::PopIOHandler(const IOHandlerSP &pop_reader_sp) {
Index: lldb/source/Interpreter/CommandInterpreter.cpp
===================================================================
--- lldb/source/Interpreter/CommandInterpreter.cpp
+++ lldb/source/Interpreter/CommandInterpreter.cpp
@@ -1854,7 +1854,7 @@
   IOHandlerConfirm *confirm =
       new IOHandlerConfirm(m_debugger, message, default_answer);
   IOHandlerSP io_handler_sp(confirm);
-  m_debugger.RunIOHandler(io_handler_sp);
+  m_debugger.PushIOHandler(io_handler_sp);
   return confirm->GetResponse();
 }
 
@@ -2477,7 +2477,11 @@
 
   m_command_source_depth++;
 
-  debugger.RunIOHandler(io_handler_sp);
+  const bool cancel_top_handler = true;
+  const bool asynchronous_if_needed = true;
+  debugger.PushIOHandler(io_handler_sp, cancel_top_handler,
+                         asynchronous_if_needed);
+
   if (!m_command_source_flags.empty())
     m_command_source_flags.pop_back();
   m_command_source_depth--;