diff --git a/Source/Android/jni/MainAndroid.cpp b/Source/Android/jni/MainAndroid.cpp
index e1b19314c3..ec7bbafd2f 100644
--- a/Source/Android/jni/MainAndroid.cpp
+++ b/Source/Android/jni/MainAndroid.cpp
@@ -124,11 +124,6 @@ void Host_RequestRenderWindowSize(int width, int height)
   jnicall.join();
 }
 
-bool Host_UINeedsControllerState()
-{
-  return true;
-}
-
 bool Host_RendererHasFocus()
 {
   return true;
diff --git a/Source/Core/Core/Core.cpp b/Source/Core/Core/Core.cpp
index 5908cc1347..a2f60badae 100644
--- a/Source/Core/Core/Core.cpp
+++ b/Source/Core/Core/Core.cpp
@@ -72,6 +72,7 @@
 #include "Core/MemoryWatcher.h"
 #endif
 
+#include "InputCommon/ControlReference/ControlReference.h"
 #include "InputCommon/ControllerInterface/ControllerInterface.h"
 #include "InputCommon/GCAdapter.h"
 
@@ -1035,4 +1036,11 @@ void DoFrameStep()
   }
 }
 
+void UpdateInputGate()
+{
+  ControlReference::SetInputGate(
+      (SConfig::GetInstance().m_BackgroundInput || Host_RendererHasFocus()) &&
+      !Host_UIBlocksControllerState());
+}
+
 }  // namespace Core
diff --git a/Source/Core/Core/Core.h b/Source/Core/Core/Core.h
index 530079b8ab..4145895faf 100644
--- a/Source/Core/Core/Core.h
+++ b/Source/Core/Core/Core.h
@@ -110,4 +110,6 @@ void HostDispatchJobs();
 
 void DoFrameStep();
 
+void UpdateInputGate();
+
 }  // namespace Core
diff --git a/Source/Core/Core/HW/VideoInterface.cpp b/Source/Core/Core/HW/VideoInterface.cpp
index 9af6f9f46a..7d78e314b9 100644
--- a/Source/Core/Core/HW/VideoInterface.cpp
+++ b/Source/Core/Core/HW/VideoInterface.cpp
@@ -737,6 +737,7 @@ void Update(u64 ticks)
 
   if (s_half_line_of_next_si_poll == s_half_line_count)
   {
+    Core::UpdateInputGate();
     SerialInterface::UpdateDevices();
     s_half_line_of_next_si_poll += 2 * SerialInterface::GetPollXLines();
   }
diff --git a/Source/Core/Core/Host.h b/Source/Core/Core/Host.h
index 99c0c61708..d3f5ee4b61 100644
--- a/Source/Core/Core/Host.h
+++ b/Source/Core/Core/Host.h
@@ -32,7 +32,6 @@ enum class HostMessageID
   WMUserJobDispatch,
 };
 
-bool Host_UINeedsControllerState();
 bool Host_UIBlocksControllerState();
 bool Host_RendererHasFocus();
 bool Host_RendererIsFullscreen();
diff --git a/Source/Core/Core/IOS/USB/USB_KBD.cpp b/Source/Core/Core/IOS/USB/USB_KBD.cpp
index 77deb65948..5f690506cb 100644
--- a/Source/Core/Core/IOS/USB/USB_KBD.cpp
+++ b/Source/Core/Core/IOS/USB/USB_KBD.cpp
@@ -212,7 +212,7 @@ IPCCommandResult USB_KBD::Write(const ReadWriteRequest& request)
 IPCCommandResult USB_KBD::IOCtl(const IOCtlRequest& request)
 {
   if (SConfig::GetInstance().m_WiiKeyboard && !Core::WantsDeterminism() &&
-      ControlReference::InputGateOn() && !m_message_queue.empty())
+      ControlReference::GetInputGate() && !m_message_queue.empty())
   {
     Memory::CopyToEmu(request.buffer_out, &m_message_queue.front(), sizeof(MessageData));
     m_message_queue.pop();
diff --git a/Source/Core/DolphinNoGUI/MainNoGUI.cpp b/Source/Core/DolphinNoGUI/MainNoGUI.cpp
index 711583f736..178501194a 100644
--- a/Source/Core/DolphinNoGUI/MainNoGUI.cpp
+++ b/Source/Core/DolphinNoGUI/MainNoGUI.cpp
@@ -82,11 +82,6 @@ void Host_RequestRenderWindowSize(int width, int height)
 {
 }
 
-bool Host_UINeedsControllerState()
-{
-  return false;
-}
-
 bool Host_RendererHasFocus()
 {
   return s_platform->IsWindowFocused();
diff --git a/Source/Core/DolphinQt/Config/Mapping/MappingIndicator.cpp b/Source/Core/DolphinQt/Config/Mapping/MappingIndicator.cpp
index a1d0eb144c..08a4f1ccb4 100644
--- a/Source/Core/DolphinQt/Config/Mapping/MappingIndicator.cpp
+++ b/Source/Core/DolphinQt/Config/Mapping/MappingIndicator.cpp
@@ -25,7 +25,6 @@
 
 #include "DolphinQt/Config/Mapping/MappingWidget.h"
 #include "DolphinQt/QtUtils/ModalMessageBox.h"
-#include "DolphinQt/Settings.h"
 
 namespace
 {
@@ -567,9 +566,6 @@ void MappingIndicator::DrawForce(ControllerEmu::Force& force)
 
 void MappingIndicator::paintEvent(QPaintEvent*)
 {
-  // TODO: The SetControllerStateNeeded interface leaks input into the game.
-  Settings::Instance().SetControllerStateNeeded(true);
-
   switch (m_group->type)
   {
   case ControllerEmu::GroupType::Cursor:
@@ -588,8 +584,6 @@ void MappingIndicator::paintEvent(QPaintEvent*)
   default:
     break;
   }
-
-  Settings::Instance().SetControllerStateNeeded(false);
 }
 
 ShakeMappingIndicator::ShakeMappingIndicator(ControllerEmu::Shake* group)
@@ -599,9 +593,7 @@ ShakeMappingIndicator::ShakeMappingIndicator(ControllerEmu::Shake* group)
 
 void ShakeMappingIndicator::paintEvent(QPaintEvent*)
 {
-  Settings::Instance().SetControllerStateNeeded(true);
   DrawShake();
-  Settings::Instance().SetControllerStateNeeded(false);
 }
 
 void ShakeMappingIndicator::DrawShake()
diff --git a/Source/Core/DolphinQt/Config/Mapping/MappingWidget.cpp b/Source/Core/DolphinQt/Config/Mapping/MappingWidget.cpp
index b9149027ea..ec4b055989 100644
--- a/Source/Core/DolphinQt/Config/Mapping/MappingWidget.cpp
+++ b/Source/Core/DolphinQt/Config/Mapping/MappingWidget.cpp
@@ -14,7 +14,6 @@
 #include "DolphinQt/Config/Mapping/MappingIndicator.h"
 #include "DolphinQt/Config/Mapping/MappingNumeric.h"
 #include "DolphinQt/Config/Mapping/MappingWindow.h"
-#include "DolphinQt/Settings.h"
 
 #include "InputCommon/ControlReference/ControlReference.h"
 #include "InputCommon/ControllerEmu/Control/Control.h"
@@ -31,11 +30,8 @@ MappingWidget::MappingWidget(MappingWindow* parent) : m_parent(parent)
 
   const auto timer = new QTimer(this);
   connect(timer, &QTimer::timeout, this, [this] {
-    // TODO: The SetControllerStateNeeded interface leaks input into the game.
     const auto lock = m_parent->GetController()->GetStateLock();
-    Settings::Instance().SetControllerStateNeeded(true);
     emit Update();
-    Settings::Instance().SetControllerStateNeeded(false);
   });
 
   timer->start(1000 / INDICATOR_UPDATE_FREQ);
diff --git a/Source/Core/DolphinQt/Host.cpp b/Source/Core/DolphinQt/Host.cpp
index ac9c91942f..fc53954195 100644
--- a/Source/Core/DolphinQt/Host.cpp
+++ b/Source/Core/DolphinQt/Host.cpp
@@ -153,12 +153,6 @@ void Host_RequestRenderWindowSize(int w, int h)
   emit Host::GetInstance()->RequestRenderSize(w, h);
 }
 
-bool Host_UINeedsControllerState()
-{
-  return Settings::Instance().IsControllerStateNeeded() ||
-         (ImGui::GetCurrentContext() && ImGui::GetIO().WantCaptureKeyboard);
-}
-
 bool Host_UIBlocksControllerState()
 {
   return ImGui::GetCurrentContext() && ImGui::GetIO().WantCaptureKeyboard;
diff --git a/Source/Core/DolphinQt/HotkeyScheduler.cpp b/Source/Core/DolphinQt/HotkeyScheduler.cpp
index b2f5c86d98..cb67fba6ea 100644
--- a/Source/Core/DolphinQt/HotkeyScheduler.cpp
+++ b/Source/Core/DolphinQt/HotkeyScheduler.cpp
@@ -25,6 +25,7 @@
 
 #include "DolphinQt/Settings.h"
 
+#include "InputCommon/ControlReference/ControlReference.h"
 #include "InputCommon/ControllerInterface/ControllerInterface.h"
 
 #include "VideoCommon/OnScreenDisplay.h"
@@ -142,8 +143,14 @@ void HotkeyScheduler::Run()
 
     if (Core::GetState() != Core::State::Stopping)
     {
+      // Obey window focus before checking hotkeys.
+      Core::UpdateInputGate();
+
       HotkeyManagerEmu::GetStatus();
 
+      // Everything else on the host thread (controller config dialog) should always get input.
+      ControlReference::SetInputGate(true);
+
       if (!Core::IsRunningAndStarted())
         continue;
 
diff --git a/Source/Core/DolphinQt/Settings.cpp b/Source/Core/DolphinQt/Settings.cpp
index 99322db7fe..cbc4849793 100644
--- a/Source/Core/DolphinQt/Settings.cpp
+++ b/Source/Core/DolphinQt/Settings.cpp
@@ -388,16 +388,6 @@ bool Settings::IsBreakpointsVisible() const
   return GetQSettings().value(QStringLiteral("debugger/showbreakpoints")).toBool();
 }
 
-bool Settings::IsControllerStateNeeded() const
-{
-  return m_controller_state_needed;
-}
-
-void Settings::SetControllerStateNeeded(bool needed)
-{
-  m_controller_state_needed = needed;
-}
-
 void Settings::SetCodeVisible(bool enabled)
 {
   if (IsCodeVisible() != enabled)
diff --git a/Source/Core/DolphinQt/Settings.h b/Source/Core/DolphinQt/Settings.h
index f16ce2a474..c9c5f1a422 100644
--- a/Source/Core/DolphinQt/Settings.h
+++ b/Source/Core/DolphinQt/Settings.h
@@ -57,8 +57,6 @@ public:
   void SetLogVisible(bool visible);
   bool IsLogConfigVisible() const;
   void SetLogConfigVisible(bool visible);
-  bool IsControllerStateNeeded() const;
-  void SetControllerStateNeeded(bool needed);
   void SetToolBarVisible(bool visible);
   bool IsToolBarVisible() const;
   void SetWidgetsLocked(bool visible);
@@ -179,7 +177,6 @@ signals:
 
 private:
   bool m_batch = false;
-  bool m_controller_state_needed = false;
   std::shared_ptr<NetPlay::NetPlayClient> m_client;
   std::shared_ptr<NetPlay::NetPlayServer> m_server;
   Settings();
diff --git a/Source/Core/InputCommon/ControlReference/ControlReference.cpp b/Source/Core/InputCommon/ControlReference/ControlReference.cpp
index af7536547c..b1dd5deee3 100644
--- a/Source/Core/InputCommon/ControlReference/ControlReference.cpp
+++ b/Source/Core/InputCommon/ControlReference/ControlReference.cpp
@@ -4,19 +4,18 @@
 
 #include "InputCommon/ControlReference/ControlReference.h"
 
-// For InputGateOn()
-// This is a bad layering violation, but it's the cleanest
-// place I could find to put it.
-#include "Core/ConfigManager.h"
-#include "Core/Host.h"
-
 using namespace ciface::ExpressionParser;
 
-bool ControlReference::InputGateOn()
+static thread_local bool tls_input_gate = true;
+
+void ControlReference::SetInputGate(bool enable)
 {
-  return (SConfig::GetInstance().m_BackgroundInput || Host_RendererHasFocus() ||
-          Host_UINeedsControllerState()) &&
-         !Host_UIBlocksControllerState();
+  tls_input_gate = enable;
+}
+
+bool ControlReference::GetInputGate()
+{
+  return tls_input_gate;
 }
 
 //
@@ -90,7 +89,7 @@ bool OutputReference::IsInput() const
 //
 ControlState InputReference::State(const ControlState ignore)
 {
-  if (m_parsed_expression && InputGateOn())
+  if (m_parsed_expression && GetInputGate())
     return m_parsed_expression->GetValue() * range;
   return 0.0;
 }
diff --git a/Source/Core/InputCommon/ControlReference/ControlReference.h b/Source/Core/InputCommon/ControlReference/ControlReference.h
index 3f2c205501..539c7f4927 100644
--- a/Source/Core/InputCommon/ControlReference/ControlReference.h
+++ b/Source/Core/InputCommon/ControlReference/ControlReference.h
@@ -22,7 +22,9 @@
 class ControlReference
 {
 public:
-  static bool InputGateOn();
+  // Note: this is per thread.
+  static void SetInputGate(bool enable);
+  static bool GetInputGate();
 
   virtual ~ControlReference();
   virtual ControlState State(const ControlState state = 0) = 0;
diff --git a/Source/DSPTool/StubHost.cpp b/Source/DSPTool/StubHost.cpp
index ac6ef92e52..75dd66296d 100644
--- a/Source/DSPTool/StubHost.cpp
+++ b/Source/DSPTool/StubHost.cpp
@@ -34,10 +34,6 @@ void Host_UpdateMainFrame()
 void Host_RequestRenderWindowSize(int, int)
 {
 }
-bool Host_UINeedsControllerState()
-{
-  return false;
-}
 bool Host_RendererHasFocus()
 {
   return false;
diff --git a/Source/UnitTests/StubHost.cpp b/Source/UnitTests/StubHost.cpp
index 440ecd336a..4fa45ef1c2 100644
--- a/Source/UnitTests/StubHost.cpp
+++ b/Source/UnitTests/StubHost.cpp
@@ -31,10 +31,6 @@ void Host_UpdateMainFrame()
 void Host_RequestRenderWindowSize(int, int)
 {
 }
-bool Host_UINeedsControllerState()
-{
-  return false;
-}
 bool Host_UIBlocksControllerState()
 {
   return false;