diff --git a/.github/workflows/ci-linux.yml b/.github/workflows/ci-linux.yml
index d74168f148e..104fd006530 100644
--- a/.github/workflows/ci-linux.yml
+++ b/.github/workflows/ci-linux.yml
@@ -160,6 +160,8 @@ jobs:
         run: |
           sudo apt-get update -y
           sudo apt-get install -y \
+            at-spi2-core \
+            dbus-x11 \
             x11-xserver-utils \
             xvfb
 
@@ -171,11 +173,30 @@ jobs:
         id: test
         working-directory: build/tests
         run: |
+          # Start D-Bus session bus
+          eval "$(dbus-launch --sh-syntax)"
+          echo "D-Bus session started with SESSION_MANAGER=${DBUS_SESSION_BUS_ADDRESS}"
+
+          # Start accessibility services
+          /usr/libexec/at-spi-bus-launcher &
+          AT_SPI_PID=$!
+
+          # Start X11 display
           export DISPLAY=:1
           Xvfb ${DISPLAY} -screen 0 1024x768x24 &
+          XVFB_PID=$!
           sleep 5  # give Xvfb time to start
 
+          # Run the tests with proper cleanup
           ./test_sunshine --gtest_color=yes --gtest_output=xml:test_results.xml
+          TEST_EXIT_CODE=$?
+
+          # Clean up background processes
+          kill "${XVFB_PID}" 2>/dev/null || true
+          kill "${AT_SPI_PID}" 2>/dev/null || true
+          kill "${DBUS_SESSION_BUS_PID}" 2>/dev/null || true
+
+          exit ${TEST_EXIT_CODE}
 
       - name: Generate gcov report
         id: test_report
diff --git a/scripts/linux_build.sh b/scripts/linux_build.sh
index bfffacb292e..8263fb31fa6 100755
--- a/scripts/linux_build.sh
+++ b/scripts/linux_build.sh
@@ -128,6 +128,8 @@ function add_arch_deps() {
     'opus'
     'udev'
     'wayland'
+    'dbus'  # D-Bus for system tray support
+    'at-spi2-core'  # AT-SPI accessibility services
   )
 
   if [ "$skip_libva" == 0 ]; then
@@ -181,6 +183,8 @@ function add_debian_based_deps() {
     "udev"
     "wget"  # necessary for cuda install with `run` file
     "xvfb"  # necessary for headless unit testing
+    "dbus-x11"  # D-Bus session bus for system tray tests
+    "at-spi2-core"  # AT-SPI accessibility services for system tray
   )
 
   if [ "$skip_libva" == 0 ]; then
@@ -251,6 +255,8 @@ function add_fedora_deps() {
     "wget"  # necessary for cuda install with `run` file
     "which"  # necessary for cuda install with `run` file
     "xorg-x11-server-Xvfb"  # necessary for headless unit testing
+    "dbus-x11"  # D-Bus session bus for system tray tests
+    "at-spi2-core"  # AT-SPI accessibility services for system tray
   )
 
   if [ "$skip_libva" == 0 ]; then
diff --git a/src/system_tray.cpp b/src/system_tray.cpp
index 812483560ef..d21ef824fdc 100644
--- a/src/system_tray.cpp
+++ b/src/system_tray.cpp
@@ -191,7 +191,7 @@ namespace system_tray {
     // Wait for the shell to be initialized before registering the tray icon.
     // This ensures the tray icon works reliably after a logoff/logon cycle.
     while (GetShellWindow() == nullptr) {
-      Sleep(1000);
+      Sleep(1000);  // TODO: this delay causes unit tests to take ~10s for each tray initialization
     }
   #endif
 
diff --git a/tests/unit/test_system_tray.cpp b/tests/unit/test_system_tray.cpp
new file mode 100644
index 00000000000..399971f34bc
--- /dev/null
+++ b/tests/unit/test_system_tray.cpp
@@ -0,0 +1,301 @@
+/**
+ * @file tests/unit/test_system_tray.cpp
+ * @brief Test src/system_tray.*.
+ */
+#include "../tests_common.h"
+#include "../tests_log_checker.h"
+
+#include <chrono>
+#include <thread>
+
+// Only test the system tray if it's enabled
+#if defined SUNSHINE_TRAY && SUNSHINE_TRAY >= 1
+
+  #include <src/system_tray.h>
+
+namespace {
+  constexpr auto log_file = "test_sunshine.log";
+
+  // Helper class to manage tray lifecycle in tests
+  class TrayTestHelper {
+  public:
+    static void cleanup_any_existing_tray() {
+      // Ensure no tray is running before starting tests
+      system_tray::end_tray();
+      system_tray::end_tray_threaded();
+    }
+  };
+}  // namespace
+
+class SystemTrayTest: public testing::Test {
+protected:
+  void SetUp() override {
+    TrayTestHelper::cleanup_any_existing_tray();
+  }
+
+  void TearDown() override {
+    TrayTestHelper::cleanup_any_existing_tray();
+  }
+};
+
+class SystemTrayThreadedTest: public testing::Test {
+protected:
+  void SetUp() override {
+    TrayTestHelper::cleanup_any_existing_tray();
+  }
+
+  void TearDown() override {
+    TrayTestHelper::cleanup_any_existing_tray();
+  }
+};
+
+// Test basic tray initialization
+TEST_F(SystemTrayTest, InitTray) {
+  // Note: This test may fail in CI environments without a display
+  // The test verifies the function doesn't crash and returns a status
+  const int result = system_tray::init_tray();
+
+  // The result should be either 0 (success) or 1 (failure, e.g., no display)
+  EXPECT_TRUE(result == 0 || result == 1);
+
+  if (result == 0) {
+    // If initialization succeeded, we should be able to clean up
+    EXPECT_EQ(0, system_tray::end_tray());
+  }
+}
+
+// Test tray event processing
+TEST_F(SystemTrayTest, ProcessTrayEvents) {
+  if (const int init_result = system_tray::init_tray(); init_result == 0) {
+    // If the tray was initialized successfully, test event processing
+    const int process_result = system_tray::process_tray_events();
+    EXPECT_EQ(0, process_result);
+
+    // Clean up
+    EXPECT_EQ(0, system_tray::end_tray());
+  } else {
+    // If no tray available, processing should fail gracefully
+    int process_result = system_tray::process_tray_events();
+    EXPECT_NE(0, process_result);
+  }
+}
+
+// Test tray update functions don't crash
+TEST_F(SystemTrayTest, UpdateTrayFunctions) {
+  const std::string test_app = "TestApp";
+
+  // These functions should not crash even if the tray is not initialized
+  EXPECT_NO_THROW(system_tray::update_tray_playing(test_app));
+  EXPECT_NO_THROW(system_tray::update_tray_pausing(test_app));
+  EXPECT_NO_THROW(system_tray::update_tray_stopped(test_app));
+  EXPECT_NO_THROW(system_tray::update_tray_require_pin());
+}
+
+// Test tray update functions with an initialized tray
+TEST_F(SystemTrayTest, UpdateTrayWithInitializedTray) {
+  if (int init_result = system_tray::init_tray(); init_result == 0) {
+    const std::string test_app = "TestApp";
+
+    // These should work without crashing when tray is initialized
+    EXPECT_NO_THROW(system_tray::update_tray_playing(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_pausing(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_stopped(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_require_pin());
+
+    // Clean up
+    EXPECT_EQ(0, system_tray::end_tray());
+  }
+}
+
+// Test ending tray without initialization
+TEST_F(SystemTrayTest, EndTrayWithoutInit) {
+  // Should be safe to call end_tray even if not initialized
+  EXPECT_EQ(0, system_tray::end_tray());
+}
+
+// Test threaded tray initialization
+TEST_F(SystemTrayThreadedTest, InitTrayThreaded) {
+  const int result = system_tray::init_tray_threaded();
+
+  // The result should be either 0 (success) or 1 (failure, e.g., no display)
+  EXPECT_TRUE(result == 0 || result == 1);
+
+  if (result == 0) {
+    // Give the thread a moment to start
+    std::this_thread::sleep_for(std::chrono::milliseconds(50));
+
+    // Verify we can stop the threaded tray
+    EXPECT_EQ(0, system_tray::end_tray_threaded());
+  }
+}
+
+// Test double initialization of a threaded tray
+TEST_F(SystemTrayThreadedTest, DoubleInitTrayThreaded) {
+  if (const int first_result = system_tray::init_tray_threaded(); first_result == 0) {
+    // Give the thread a moment to start
+    std::this_thread::sleep_for(std::chrono::milliseconds(100));
+
+    // Second initialization should fail
+    const int second_result = system_tray::init_tray_threaded();
+    EXPECT_EQ(1, second_result);
+
+    // Check that a warning message was logged
+    EXPECT_TRUE(log_checker::line_contains(log_file, "Tray thread is already running"));
+
+    // Clean up
+    EXPECT_EQ(0, system_tray::end_tray_threaded());
+  }
+}
+
+// Test ending threaded tray without initialization
+TEST_F(SystemTrayThreadedTest, EndThreadedTrayWithoutInit) {
+  // Should be safe to call end_tray_threaded even if not initialized
+  EXPECT_EQ(0, system_tray::end_tray_threaded());
+}
+
+// Test threaded tray lifecycle
+TEST_F(SystemTrayThreadedTest, ThreadedTrayLifecycle) {
+  if (int init_result = system_tray::init_tray_threaded(); init_result == 0) {
+    // Give the thread time to start and initialize
+    std::this_thread::sleep_for(std::chrono::milliseconds(200));
+
+    // Check that an initialization message was logged
+    EXPECT_TRUE(log_checker::line_contains(log_file, "System tray thread initialized successfully"));
+
+    // Test tray updates work with a threaded tray
+    const std::string test_app = "ThreadedTestApp";
+    EXPECT_NO_THROW(system_tray::update_tray_playing(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_pausing(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_stopped(test_app));
+    EXPECT_NO_THROW(system_tray::update_tray_require_pin());
+
+    // Stop the threaded tray
+    EXPECT_EQ(0, system_tray::end_tray_threaded());
+
+    // Give the thread time to stop
+    std::this_thread::sleep_for(std::chrono::milliseconds(100));
+
+    // Check that a stop message was logged
+    EXPECT_TRUE(log_checker::line_contains(log_file, "System tray thread stopped"));
+  }
+}
+
+// Test that main-thread and threaded tray don't interfere
+TEST_F(SystemTrayTest, MainThreadAndThreadedTrayIsolation) {
+  // Initialize a main thread tray first
+
+  if (const int main_result = system_tray::init_tray(); main_result == 0) {
+    // Try to initialize threaded tray - should work independently
+
+    if (const int threaded_result = system_tray::init_tray_threaded(); threaded_result == 0) {
+      // Give a threaded tray time to start
+      std::this_thread::sleep_for(std::chrono::milliseconds(100));
+
+      // Both should be able to clean up independently
+      EXPECT_EQ(0, system_tray::end_tray());
+      EXPECT_EQ(0, system_tray::end_tray_threaded());
+    } else {
+      // Clean up the main thread tray
+      EXPECT_EQ(0, system_tray::end_tray());
+    }
+  }
+}
+
+// Test rapid start/stop cycles
+TEST_F(SystemTrayThreadedTest, RapidStartStopCycles) {
+  // First, check if tray initialization is possible in this environment
+  BOOST_LOG(info) << "Testing tray initialization capability...";
+
+  if (const int test_init_result = system_tray::init_tray_threaded(); test_init_result != 0) {
+    // Try a regular tray initialization to see if it's a threading issue
+    if (const int regular_init_result = system_tray::init_tray(); regular_init_result == 0) {
+      BOOST_LOG(info) << "Regular tray initialization succeeded, but threaded failed";
+      system_tray::end_tray();
+      GTEST_SKIP() << "Threaded tray initialization failed (code: " << test_init_result
+                   << "), but regular tray works. May be a threading/timing issue in test environment.";
+    } else {
+      BOOST_LOG(info) << "Both regular and threaded tray initialization failed - no display available";
+      // Instead of skipping, let's test the threading logic without actual tray
+      BOOST_LOG(info) << "Testing threading functionality without display...";
+
+      // Test that the threading functions don't crash and return appropriate error codes
+      EXPECT_EQ(1, test_init_result);  // Should fail with code 1 (no display)
+      EXPECT_EQ(1, regular_init_result);  // Should fail with code 1 (no display)
+
+      // Test multiple calls to init_tray_threaded when no display is available
+      const int second_init_result = system_tray::init_tray_threaded();
+      EXPECT_EQ(1, second_init_result);  // Should consistently fail
+
+      // Test that end_tray_threaded is safe to call even when init failed
+      EXPECT_EQ(0, system_tray::end_tray_threaded());  // Should always return 0
+
+      // Test that update functions don't crash when no tray is available
+      const std::string test_app = "NoDisplayTestApp";
+      EXPECT_NO_THROW(system_tray::update_tray_playing(test_app));
+      EXPECT_NO_THROW(system_tray::update_tray_pausing(test_app));
+      EXPECT_NO_THROW(system_tray::update_tray_stopped(test_app));
+      EXPECT_NO_THROW(system_tray::update_tray_require_pin());
+
+      BOOST_LOG(info) << "Threading functionality tested successfully (no display mode)";
+      return;  // Test passed - we validated the threading logic works correctly
+    }
+  }
+
+  BOOST_LOG(info) << "Tray initialization succeeded, proceeding with controlled cycles test";
+
+  // Clean up the test initialization
+  EXPECT_EQ(0, system_tray::end_tray_threaded());
+
+  // Note: The Windows system tray has limitations on rapid reinitialization
+  std::this_thread::sleep_for(std::chrono::milliseconds(1000));  // Longer wait for full cleanup
+  BOOST_LOG(info) << "Starting controlled start/stop cycle";
+
+  if (const int init_result = system_tray::init_tray_threaded(); init_result == 0) {
+    BOOST_LOG(info) << "Cycle completed successfully - threaded tray can be reinitialized";
+
+    // Give the thread time to start properly
+    std::this_thread::sleep_for(std::chrono::milliseconds(200));
+
+    // Test some tray operations while it's running
+    const std::string test_app = "CycleTestApp";
+    EXPECT_NO_THROW(system_tray::update_tray_playing(test_app));
+    std::this_thread::sleep_for(std::chrono::milliseconds(100));
+
+    EXPECT_NO_THROW(system_tray::update_tray_stopped(test_app));
+    std::this_thread::sleep_for(std::chrono::milliseconds(100));
+
+    // Stop the tray
+    const int stop_result = system_tray::end_tray_threaded();
+    EXPECT_EQ(0, stop_result);
+
+    BOOST_LOG(info) << "Controlled cycle test completed successfully";
+  } else {
+    FAIL() << "Tray reinitialization not supported in this environment. "
+           << "Initial test passed but subsequent initialization failed with code: " << init_result;
+  }
+}
+
+// Performance test - verify thread startup time is reasonable
+TEST_F(SystemTrayThreadedTest, ThreadStartupPerformance) {
+  const auto start_time = std::chrono::steady_clock::now();
+
+  const int result = system_tray::init_tray_threaded();
+
+  const auto end_time = std::chrono::steady_clock::now();
+  const auto duration = std::chrono::duration_cast<std::chrono::milliseconds>(end_time - start_time);
+
+  if (result == 0) {
+    // Startup should complete within 5 seconds (much less in practice)
+    EXPECT_LT(duration.count(), 5000);
+
+    // Clean up
+    EXPECT_EQ(0, system_tray::end_tray_threaded());
+  }
+}
+
+#else
+// If the tray is not enabled, provide a simple test that passes
+TEST(SystemTrayDisabled, TrayNotEnabled) {
+  GTEST_SKIP() << "System tray is not enabled in this build";
+}
+#endif