diff --git a/src/duckstation-qt/debuggerwindow.cpp b/src/duckstation-qt/debuggerwindow.cpp
index 8f7c45b34..54d8e8ee6 100644
--- a/src/duckstation-qt/debuggerwindow.cpp
+++ b/src/duckstation-qt/debuggerwindow.cpp
@@ -1,12 +1,14 @@
-// SPDX-FileCopyrightText: 2019-2022 Connor McLaughlin <stenzek@gmail.com>
+// SPDX-FileCopyrightText: 2019-2024 Connor McLaughlin <stenzek@gmail.com>
 // SPDX-License-Identifier: (GPL-3.0 OR CC-BY-NC-ND-4.0)
 
 #include "debuggerwindow.h"
-#include "common/assert.h"
-#include "core/cpu_core_private.h"
 #include "debuggermodels.h"
 #include "qthost.h"
 #include "qtutils.h"
+
+#include "common/assert.h"
+#include "core/cpu_core_private.h"
+
 #include <QtCore/QSignalBlocker>
 #include <QtGui/QFontDatabase>
 #include <QtWidgets/QFileDialog>
@@ -20,14 +22,24 @@ DebuggerWindow::DebuggerWindow(QWidget* parent /* = nullptr */)
   connectSignals();
   createModels();
   setMemoryViewRegion(Bus::MemoryRegion::RAM);
-  setUIEnabled(false);
+  setUIEnabled(QtHost::IsSystemPaused(), QtHost::IsSystemValid());
 }
 
 DebuggerWindow::~DebuggerWindow() = default;
 
-void DebuggerWindow::onEmulationPaused()
+void DebuggerWindow::onSystemStarted()
 {
-  setUIEnabled(true);
+  setUIEnabled(false, true);
+}
+
+void DebuggerWindow::onSystemDestroyed()
+{
+  setUIEnabled(false, false);
+}
+
+void DebuggerWindow::onSystemPaused()
+{
+  setUIEnabled(true, true);
   refreshAll();
   refreshBreakpointList();
 
@@ -37,9 +49,9 @@ void DebuggerWindow::onEmulationPaused()
   }
 }
 
-void DebuggerWindow::onEmulationResumed()
+void DebuggerWindow::onSystemResumed()
 {
-  setUIEnabled(false);
+  setUIEnabled(false, true);
 
   {
     QSignalBlocker sb(m_ui.actionPause);
@@ -84,7 +96,7 @@ void DebuggerWindow::onPauseActionToggled(bool paused)
   if (!paused)
   {
     m_registers_model->saveCurrentValues();
-    setUIEnabled(false);
+    setUIEnabled(false, true);
   }
 
   g_emu_thread->setSystemPaused(paused);
@@ -422,8 +434,10 @@ void DebuggerWindow::setupAdditionalUi()
 
 void DebuggerWindow::connectSignals()
 {
-  connect(g_emu_thread, &EmuThread::systemPaused, this, &DebuggerWindow::onEmulationPaused);
-  connect(g_emu_thread, &EmuThread::systemResumed, this, &DebuggerWindow::onEmulationResumed);
+  connect(g_emu_thread, &EmuThread::systemPaused, this, &DebuggerWindow::onSystemPaused);
+  connect(g_emu_thread, &EmuThread::systemResumed, this, &DebuggerWindow::onSystemResumed);
+  connect(g_emu_thread, &EmuThread::systemStarted, this, &DebuggerWindow::onSystemStarted);
+  connect(g_emu_thread, &EmuThread::systemDestroyed, this, &DebuggerWindow::onSystemDestroyed);
   connect(g_emu_thread, &EmuThread::debuggerMessageReported, this, &DebuggerWindow::onDebuggerMessageReported);
 
   connect(m_ui.actionPause, &QAction::toggled, this, &DebuggerWindow::onPauseActionToggled);
@@ -483,8 +497,10 @@ void DebuggerWindow::createModels()
   m_ui.breakpointsWidget->setRootIsDecorated(false);
 }
 
-void DebuggerWindow::setUIEnabled(bool enabled)
+void DebuggerWindow::setUIEnabled(bool enabled, bool allow_pause)
 {
+  m_ui.actionPause->setEnabled(allow_pause);
+
   // Disable all UI elements that depend on execution state
   m_ui.codeView->setEnabled(enabled);
   m_ui.registerView->setEnabled(enabled);
diff --git a/src/duckstation-qt/debuggerwindow.h b/src/duckstation-qt/debuggerwindow.h
index c4cbc54f1..7b47e21de 100644
--- a/src/duckstation-qt/debuggerwindow.h
+++ b/src/duckstation-qt/debuggerwindow.h
@@ -1,9 +1,12 @@
-// SPDX-FileCopyrightText: 2019-2022 Connor McLaughlin <stenzek@gmail.com>
+// SPDX-FileCopyrightText: 2019-2024 Connor McLaughlin <stenzek@gmail.com>
 // SPDX-License-Identifier: (GPL-3.0 OR CC-BY-NC-ND-4.0)
 
 #pragma once
-#include "core/types.h"
+
 #include "ui_debuggerwindow.h"
+
+#include "core/types.h"
+
 #include <QtWidgets/QMainWindow>
 #include <memory>
 #include <optional>
@@ -27,14 +30,14 @@ public:
 Q_SIGNALS:
   void closed();
 
-public Q_SLOTS:
-  void onEmulationPaused();
-  void onEmulationResumed();
-
 protected:
   void closeEvent(QCloseEvent* event);
 
 private Q_SLOTS:
+  void onSystemStarted();
+  void onSystemDestroyed();
+  void onSystemPaused();
+  void onSystemResumed();
   void onDebuggerMessageReported(const QString& message);
 
   void refreshAll();
@@ -47,7 +50,7 @@ private Q_SLOTS:
   void onGoToAddressTriggered();
   void onDumpAddressTriggered();
   void onFollowAddressTriggered();
-  void onTraceTriggered();  
+  void onTraceTriggered();
   void onAddBreakpointTriggered();
   void onToggleBreakpointTriggered();
   void onClearBreakpointsTriggered();
@@ -59,13 +62,12 @@ private Q_SLOTS:
   void onMemorySearchTriggered();
   void onMemorySearchStringChanged(const QString&);
 
-
 private:
   void setupAdditionalUi();
   void connectSignals();
   void disconnectSignals();
   void createModels();
-  void setUIEnabled(bool enabled);
+  void setUIEnabled(bool enabled, bool allow_pause);
   void setMemoryViewRegion(Bus::MemoryRegion region);
   void toggleBreakpoint(VirtualMemoryAddress address);
   void clearBreakpoints();
diff --git a/src/duckstation-qt/mainwindow.cpp b/src/duckstation-qt/mainwindow.cpp
index 6cff789dc..aaa035332 100644
--- a/src/duckstation-qt/mainwindow.cpp
+++ b/src/duckstation-qt/mainwindow.cpp
@@ -608,12 +608,6 @@ void MainWindow::onSystemDestroyed()
     delete m_cheat_manager_dialog;
     m_cheat_manager_dialog = nullptr;
   }
-
-  if (m_debugger_window)
-  {
-    delete m_debugger_window;
-    m_debugger_window = nullptr;
-  }
 }
 
 void MainWindow::onRunningGameChanged(const QString& filename, const QString& game_serial, const QString& game_title)
@@ -1733,7 +1727,7 @@ void MainWindow::updateEmulationActions(bool starting, bool running, bool cheevo
   m_ui.menuChangeDisc->setDisabled(starting || !running);
   m_ui.menuCheats->setDisabled(starting || !running || cheevos_challenge_mode);
   m_ui.actionCheatManager->setDisabled(starting || !running || cheevos_challenge_mode);
-  m_ui.actionCPUDebugger->setDisabled(starting || !running || cheevos_challenge_mode);
+  m_ui.actionCPUDebugger->setDisabled(cheevos_challenge_mode);
   m_ui.actionDumpRAM->setDisabled(starting || !running || cheevos_challenge_mode);
   m_ui.actionDumpVRAM->setDisabled(starting || !running || cheevos_challenge_mode);
   m_ui.actionDumpSPURAM->setDisabled(starting || !running || cheevos_challenge_mode);
@@ -2871,19 +2865,19 @@ void MainWindow::onToolsCheatManagerTriggered()
 
 void MainWindow::openCPUDebugger()
 {
-  g_emu_thread->setSystemPaused(true, true);
-  if (!System::IsValid())
+  if (m_debugger_window)
+  {
+    m_debugger_window->raise();
+    m_debugger_window->activateWindow();
+    m_debugger_window->setFocus();
     return;
+  }
 
   Assert(!m_debugger_window);
-
   m_debugger_window = new DebuggerWindow();
   m_debugger_window->setWindowIcon(windowIcon());
   connect(m_debugger_window, &DebuggerWindow::closed, this, &MainWindow::onCPUDebuggerClosed);
   m_debugger_window->show();
-
-  // the debugger will miss the pause event above (or we were already paused), so fire it now
-  m_debugger_window->onEmulationPaused();
 }
 
 void MainWindow::onCPUDebuggerClosed()