diff --git a/Source/Core/DolphinQt/RenderWidget.cpp b/Source/Core/DolphinQt/RenderWidget.cpp
index a534905056..cb55877ace 100644
--- a/Source/Core/DolphinQt/RenderWidget.cpp
+++ b/Source/Core/DolphinQt/RenderWidget.cpp
@@ -397,9 +397,11 @@ bool RenderWidget::event(QEvent* event)
   // Note that this event in Windows is not always aligned to the window that is highlighted,
   // it's the window that has keyboard and mouse focus
   case QEvent::WindowActivate:
-    if (Config::Get(Config::MAIN_PAUSE_ON_FOCUS_LOST) && Core::GetState() == Core::State::Paused)
+    if (m_should_unpause_on_focus && Core::GetState() == Core::State::Paused)
       Core::SetState(Core::State::Running);
 
+    m_should_unpause_on_focus = false;
+
     UpdateCursor();
 
     // Avoid "race conditions" with message boxes
@@ -425,7 +427,10 @@ bool RenderWidget::event(QEvent* event)
       // is waiting for us to finish showing a panic alert (with that panic alert likely being
       // the cause of this event), so trying to pause the core would cause a deadlock
       if (!Core::IsCPUThread() && !Core::IsGPUThread())
+      {
+        m_should_unpause_on_focus = true;
         Core::SetState(Core::State::Paused);
+      }
     }
 
     emit FocusChanged(false);
diff --git a/Source/Core/DolphinQt/RenderWidget.h b/Source/Core/DolphinQt/RenderWidget.h
index c44f673cb2..c8ea1e3a84 100644
--- a/Source/Core/DolphinQt/RenderWidget.h
+++ b/Source/Core/DolphinQt/RenderWidget.h
@@ -51,4 +51,5 @@ private:
   bool m_lock_cursor_on_next_activation = false;
   bool m_dont_lock_cursor_on_show = false;
   bool m_waiting_for_message_box = false;
+  bool m_should_unpause_on_focus = false;
 };