diff --git a/app/gui/StreamSegue.qml b/app/gui/StreamSegue.qml
index b3b0fd42..52cd9887 100644
--- a/app/gui/StreamSegue.qml
+++ b/app/gui/StreamSegue.qml
@@ -76,10 +76,8 @@ Item {
             streamSegueErrorDialog.text += "\n\n" + qsTr("This PC's Internet connection is blocking Moonlight. Streaming over the Internet may not work while connected to this network.")
         }
 
-        if (window.gamepadInputActive) {
-            // Re-enable GUI gamepad usage now
-            SdlGamepadKeyNavigation.enable()
-        }
+        // Re-enable GUI gamepad usage now
+        SdlGamepadKeyNavigation.enable()
 
         if (quitAfter) {
             if (streamSegueErrorDialog.text) {
@@ -121,10 +119,8 @@ Item {
         // Show the toolbar again when popped off the stack
         toolBar.visible = true
 
-        if (window.gamepadInputActive) {
-            // Re-enable GUI gamepad usage now
-            SdlGamepadKeyNavigation.enable()
-        }
+        // Re-enable GUI gamepad usage now
+        SdlGamepadKeyNavigation.enable()
     }
 
     StackView.onActivated: {
diff --git a/app/gui/main.qml b/app/gui/main.qml
index 51d4b2db..bab9ecea 100644
--- a/app/gui/main.qml
+++ b/app/gui/main.qml
@@ -12,7 +12,6 @@ import SdlGamepadKeyNavigation 1.0
 
 ApplicationWindow {
     property bool pollingActive: false
-    property bool gamepadInputActive: false
 
     // Set by SettingsView to force the back operation to pop all
     // pages except the initial view. This is required when doing
@@ -33,7 +32,6 @@ ApplicationWindow {
         }
 
         SdlGamepadKeyNavigation.enable()
-        gamepadInputActive = true
     }
 
     Component.onCompleted: {
@@ -160,11 +158,6 @@ ApplicationWindow {
                 ComputerManager.stopPollingAsync()
                 pollingActive = false
             }
-
-            if (gamepadInputActive) {
-                SdlGamepadKeyNavigation.disable()
-                gamepadInputActive = false
-            }
         }
         else if (active) {
             // When we become visible and active again, start polling
@@ -175,11 +168,10 @@ ApplicationWindow {
                 ComputerManager.startPolling()
                 pollingActive = true
             }
-            if (!gamepadInputActive) {
-                SdlGamepadKeyNavigation.enable()
-                gamepadInputActive = true
-            }
         }
+
+        // Poll for gamepad input only when the window is in focus
+        SdlGamepadKeyNavigation.notifyWindowFocus(visible && active)
     }
 
     onActiveChanged: {
@@ -192,23 +184,15 @@ ApplicationWindow {
                 ComputerManager.startPolling()
                 pollingActive = true
             }
-            if (!gamepadInputActive) {
-                SdlGamepadKeyNavigation.enable()
-                gamepadInputActive = true
-            }
         }
         else {
             // Start the inactivity timer to stop polling
             // if focus does not return within a few minutes.
             inactivityTimer.restart()
-
-            // Immediately stop gamepad input since we aren't
-            // the active window anymore.
-            if (gamepadInputActive) {
-                SdlGamepadKeyNavigation.disable()
-                gamepadInputActive = false
-            }
         }
+
+        // Poll for gamepad input only when the window is in focus
+        SdlGamepadKeyNavigation.notifyWindowFocus(visible && active)
     }
 
     // Workaround for lack of instanceof in Qt 5.9.
diff --git a/app/gui/sdlgamepadkeynavigation.cpp b/app/gui/sdlgamepadkeynavigation.cpp
index e51eb776..c10ae4dd 100644
--- a/app/gui/sdlgamepadkeynavigation.cpp
+++ b/app/gui/sdlgamepadkeynavigation.cpp
@@ -13,6 +13,7 @@ SdlGamepadKeyNavigation::SdlGamepadKeyNavigation(StreamingPreferences* prefs)
       m_Enabled(false),
       m_UiNavMode(false),
       m_FirstPoll(false),
+      m_HasFocus(false),
       m_LastAxisNavigationEventTime(0)
 {
     m_PollingTimer = new QTimer(this);
@@ -63,13 +64,10 @@ void SdlGamepadKeyNavigation::enable()
         }
     }
 
-    // Flush events on the first poll
-    m_FirstPoll = true;
-
-    // Poll every 50 ms for a new joystick event
-    m_PollingTimer->start(50);
-
     m_Enabled = true;
+
+    // Start the polling timer if the window is focused
+    updateTimerState();
 }
 
 void SdlGamepadKeyNavigation::disable()
@@ -78,7 +76,9 @@ void SdlGamepadKeyNavigation::disable()
         return;
     }
 
-    m_PollingTimer->stop();
+    m_Enabled = false;
+    updateTimerState();
+    Q_ASSERT(!m_PollingTimer->isActive());
 
     while (!m_Gamepads.isEmpty()) {
         SDL_GameControllerClose(m_Gamepads[0]);
@@ -86,8 +86,12 @@ void SdlGamepadKeyNavigation::disable()
     }
 
     SDL_QuitSubSystem(SDL_INIT_GAMECONTROLLER);
+}
 
-    m_Enabled = false;
+void SdlGamepadKeyNavigation::notifyWindowFocus(bool hasFocus)
+{
+    m_HasFocus = hasFocus;
+    updateTimerState();
 }
 
 void SdlGamepadKeyNavigation::onPollingTimerFired()
@@ -261,6 +265,20 @@ void SdlGamepadKeyNavigation::sendKey(QEvent::Type type, Qt::Key key, Qt::Keyboa
     }
 }
 
+void SdlGamepadKeyNavigation::updateTimerState()
+{
+    if (m_PollingTimer->isActive() && (!m_HasFocus || !m_Enabled)) {
+        m_PollingTimer->stop();
+    }
+    else if (!m_PollingTimer->isActive() && m_HasFocus && m_Enabled) {
+        // Flush events on the first poll
+        m_FirstPoll = true;
+
+        // Poll every 50 ms for a new joystick event
+        m_PollingTimer->start(50);
+    }
+}
+
 void SdlGamepadKeyNavigation::setUiNavMode(bool uiNavMode)
 {
     m_UiNavMode = uiNavMode;
diff --git a/app/gui/sdlgamepadkeynavigation.h b/app/gui/sdlgamepadkeynavigation.h
index af283be1..7c26526a 100644
--- a/app/gui/sdlgamepadkeynavigation.h
+++ b/app/gui/sdlgamepadkeynavigation.h
@@ -20,6 +20,8 @@ public:
 
     Q_INVOKABLE void disable();
 
+    Q_INVOKABLE void notifyWindowFocus(bool hasFocus);
+
     Q_INVOKABLE void setUiNavMode(bool settingsMode);
 
     Q_INVOKABLE int getConnectedGamepads();
@@ -27,6 +29,8 @@ public:
 private:
     void sendKey(QEvent::Type type, Qt::Key key, Qt::KeyboardModifiers modifiers = Qt::NoModifier);
 
+    void updateTimerState();
+
 private slots:
     void onPollingTimerFired();
 
@@ -37,5 +41,6 @@ private:
     bool m_Enabled;
     bool m_UiNavMode;
     bool m_FirstPoll;
+    bool m_HasFocus;
     Uint32 m_LastAxisNavigationEventTime;
 };