diff --git a/packages/SystemUI/aconfig/systemui.aconfig b/packages/SystemUI/aconfig/systemui.aconfig
index f5c4843..ba77380 100644
--- a/packages/SystemUI/aconfig/systemui.aconfig
+++ b/packages/SystemUI/aconfig/systemui.aconfig
@@ -542,6 +542,13 @@
     namespace: "systemui"
     description: "Binds Keyguard Media Controller Visibility to MediaContainerView"
     bug: "298213983"
+}
+
+flag {
+    name: "delayed_wakelock_release_on_background_thread"
+    namespace: "systemui"
+    description: "Released delayed wakelocks on background threads to avoid janking screen transitions."
+    bug: "316128516"
     metadata {
         purpose: PURPOSE_BUGFIX
     }
diff --git a/packages/SystemUI/multivalentTests/src/com/android/systemui/util/wakelock/ClientTrackingWakeLockTest.kt b/packages/SystemUI/multivalentTests/src/com/android/systemui/util/wakelock/ClientTrackingWakeLockTest.kt
new file mode 100644
index 0000000..fdfcdc4
--- /dev/null
+++ b/packages/SystemUI/multivalentTests/src/com/android/systemui/util/wakelock/ClientTrackingWakeLockTest.kt
@@ -0,0 +1,130 @@
+/*
+ * Copyright (C) 2024 The Android Open Source Project
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *      http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+package com.android.systemui.util.wakelock
+
+import android.os.Build
+import android.os.PowerManager
+import androidx.test.ext.junit.runners.AndroidJUnit4
+import androidx.test.filters.SmallTest
+import com.android.systemui.SysuiTestCase
+import org.junit.After
+import org.junit.Assert
+import org.junit.Assume
+import org.junit.Before
+import org.junit.Test
+import org.junit.runner.RunWith
+
+@SmallTest
+@RunWith(AndroidJUnit4::class)
+class ClientTrackingWakeLockTest : SysuiTestCase() {
+
+    private val WHY = "test"
+    private val WHY_2 = "test2"
+
+    lateinit var mWakeLock: ClientTrackingWakeLock
+    lateinit var mInner: PowerManager.WakeLock
+
+    @Before
+    fun setUp() {
+        mInner =
+            WakeLock.createWakeLockInner(mContext, "WakeLockTest", PowerManager.PARTIAL_WAKE_LOCK)
+        mWakeLock = ClientTrackingWakeLock(mInner, null, 20000)
+    }
+
+    @After
+    fun tearDown() {
+        mInner.setReferenceCounted(false)
+        mInner.release()
+    }
+
+    @Test
+    fun createPartialInner_notHeldYet() {
+        Assert.assertFalse(mInner.isHeld)
+    }
+
+    @Test
+    fun wakeLock_acquire() {
+        mWakeLock.acquire(WHY)
+        Assert.assertTrue(mInner.isHeld)
+    }
+
+    @Test
+    fun wakeLock_release() {
+        mWakeLock.acquire(WHY)
+        mWakeLock.release(WHY)
+        Assert.assertFalse(mInner.isHeld)
+    }
+
+    @Test
+    fun wakeLock_acquiredReleasedMultipleSources_stillHeld() {
+        mWakeLock.acquire(WHY)
+        mWakeLock.acquire(WHY_2)
+        mWakeLock.release(WHY)
+
+        Assert.assertTrue(mInner.isHeld)
+        mWakeLock.release(WHY_2)
+        Assert.assertFalse(mInner.isHeld)
+    }
+
+    @Test
+    fun wakeLock_releasedTooManyTimes_stillReleased_noThrow() {
+        Assume.assumeFalse(Build.IS_ENG)
+        mWakeLock.acquire(WHY)
+        mWakeLock.acquire(WHY_2)
+        mWakeLock.release(WHY)
+        mWakeLock.release(WHY_2)
+        mWakeLock.release(WHY)
+        Assert.assertFalse(mInner.isHeld)
+    }
+
+    @Test
+    fun wakeLock_wrap() {
+        val ran = BooleanArray(1)
+        val wrapped = mWakeLock.wrap { ran[0] = true }
+        Assert.assertTrue(mInner.isHeld)
+        Assert.assertFalse(ran[0])
+        wrapped.run()
+        Assert.assertTrue(ran[0])
+        Assert.assertFalse(mInner.isHeld)
+    }
+
+    @Test
+    fun prodBuild_wakeLock_releaseWithoutAcquire_noThrow() {
+        Assume.assumeFalse(Build.IS_ENG)
+        // shouldn't throw an exception on production builds
+        mWakeLock.release(WHY)
+    }
+
+    @Test
+    fun acquireSeveralLocks_stringReportsCorrectCount() {
+        mWakeLock.acquire(WHY)
+        mWakeLock.acquire(WHY_2)
+        mWakeLock.acquire(WHY)
+        mWakeLock.acquire(WHY)
+        mWakeLock.acquire(WHY_2)
+        Assert.assertEquals(5, mWakeLock.activeClients())
+
+        mWakeLock.release(WHY_2)
+        mWakeLock.release(WHY_2)
+        Assert.assertEquals(3, mWakeLock.activeClients())
+
+        mWakeLock.release(WHY)
+        mWakeLock.release(WHY)
+        mWakeLock.release(WHY)
+        Assert.assertEquals(0, mWakeLock.activeClients())
+    }
+}
diff --git a/packages/SystemUI/src/com/android/systemui/util/wakelock/ClientTrackingWakeLock.kt b/packages/SystemUI/src/com/android/systemui/util/wakelock/ClientTrackingWakeLock.kt
new file mode 100644
index 0000000..db300eb
--- /dev/null
+++ b/packages/SystemUI/src/com/android/systemui/util/wakelock/ClientTrackingWakeLock.kt
@@ -0,0 +1,63 @@
+/*
+ * Copyright (C) 2024 The Android Open Source Project
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *      http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+package com.android.systemui.util.wakelock
+
+import android.os.PowerManager
+import android.util.Log
+import java.util.concurrent.ConcurrentHashMap
+import java.util.concurrent.atomic.AtomicInteger
+
+/**
+ * [PowerManager.WakeLock] wrapper that tracks acquire/release reasons and logs them if owning
+ * logger is enabled.
+ */
+class ClientTrackingWakeLock(
+    private val pmWakeLock: PowerManager.WakeLock,
+    private val logger: WakeLockLogger?,
+    private val maxTimeout: Long
+) : WakeLock {
+
+    private val activeClients = ConcurrentHashMap<String, AtomicInteger>()
+
+    override fun acquire(why: String) {
+        val count = activeClients.computeIfAbsent(why) { _ -> AtomicInteger(0) }.incrementAndGet()
+        logger?.logAcquire(pmWakeLock, why, count)
+        pmWakeLock.acquire(maxTimeout)
+    }
+
+    override fun release(why: String) {
+        val count = activeClients[why]?.decrementAndGet() ?: -1
+        if (count < 0) {
+            Log.wtf(WakeLock.TAG, "Releasing WakeLock with invalid reason: $why")
+            // Restore count just in case.
+            activeClients[why]?.incrementAndGet()
+            return
+        }
+
+        logger?.logRelease(pmWakeLock, why, count)
+        pmWakeLock.release()
+    }
+
+    override fun wrap(r: Runnable): Runnable = WakeLock.wrapImpl(this, r)
+
+    fun activeClients(): Int =
+        activeClients.reduceValuesToInt(Long.MAX_VALUE, AtomicInteger::get, 0, Integer::sum)
+
+    override fun toString(): String {
+        return "active clients=${activeClients()}"
+    }
+}
diff --git a/packages/SystemUI/src/com/android/systemui/util/wakelock/DelayedWakeLock.java b/packages/SystemUI/src/com/android/systemui/util/wakelock/DelayedWakeLock.java
index 039109e..d2ed71c 100644
--- a/packages/SystemUI/src/com/android/systemui/util/wakelock/DelayedWakeLock.java
+++ b/packages/SystemUI/src/com/android/systemui/util/wakelock/DelayedWakeLock.java
@@ -19,8 +19,11 @@
 import android.content.Context;
 import android.os.Handler;
 
+import com.android.systemui.Flags;
 import com.android.systemui.dagger.qualifiers.Background;
+import com.android.systemui.dagger.qualifiers.Main;
 
+import dagger.Lazy;
 import dagger.assisted.Assisted;
 import dagger.assisted.AssistedFactory;
 import dagger.assisted.AssistedInject;
@@ -37,10 +40,13 @@
     private final WakeLock mInner;
 
     @AssistedInject
-    public DelayedWakeLock(@Background Handler handler, Context context, WakeLockLogger logger,
+    public DelayedWakeLock(@Background Lazy<Handler> bgHandler,
+                           @Main Lazy<Handler> mainHandler,
+                           Context context, WakeLockLogger logger,
             @Assisted String tag) {
         mInner = WakeLock.createPartial(context, logger, tag);
-        mHandler = handler;
+        mHandler = Flags.delayedWakelockReleaseOnBackgroundThread() ? bgHandler.get()
+                : mainHandler.get();
     }
 
     @Override
diff --git a/packages/SystemUI/src/com/android/systemui/util/wakelock/WakeLock.java b/packages/SystemUI/src/com/android/systemui/util/wakelock/WakeLock.java
index 6128fee..707751a 100644
--- a/packages/SystemUI/src/com/android/systemui/util/wakelock/WakeLock.java
+++ b/packages/SystemUI/src/com/android/systemui/util/wakelock/WakeLock.java
@@ -22,6 +22,8 @@
 
 import androidx.annotation.VisibleForTesting;
 
+import com.android.systemui.Flags;
+
 import java.util.HashMap;
 
 import javax.inject.Inject;
@@ -112,6 +114,11 @@
     @VisibleForTesting
     static WakeLock wrap(
             final PowerManager.WakeLock inner, WakeLockLogger logger, long maxTimeout) {
+        if (Flags.delayedWakelockReleaseOnBackgroundThread()) {
+            return new ClientTrackingWakeLock(inner, logger, maxTimeout);
+        }
+
+        // Non-thread safe implementation, remove when flag above is removed.
         return new WakeLock() {
             private final HashMap<String, Integer> mActiveClients = new HashMap<>();
 
diff --git a/packages/SystemUI/tests/src/com/android/systemui/util/wakelock/WakeLockTest.java b/packages/SystemUI/tests/src/com/android/systemui/util/wakelock/WakeLockTest.java
index 23a9207..ed07ad2 100644
--- a/packages/SystemUI/tests/src/com/android/systemui/util/wakelock/WakeLockTest.java
+++ b/packages/SystemUI/tests/src/com/android/systemui/util/wakelock/WakeLockTest.java
@@ -21,21 +21,40 @@
 
 import android.os.Build;
 import android.os.PowerManager;
+import android.platform.test.flag.junit.FlagsParameterization;
+import android.platform.test.flag.junit.SetFlagsRule;
 
 import androidx.test.filters.SmallTest;
-import androidx.test.runner.AndroidJUnit4;
 
+import com.android.systemui.Flags;
 import com.android.systemui.SysuiTestCase;
 
 import org.junit.After;
+import org.junit.Assume;
 import org.junit.Before;
+import org.junit.Rule;
 import org.junit.Test;
 import org.junit.runner.RunWith;
+import org.junit.runners.Parameterized;
+
+import java.util.List;
 
 @SmallTest
-@RunWith(AndroidJUnit4.class)
+@RunWith(Parameterized.class)
 public class WakeLockTest extends SysuiTestCase {
 
+    @Parameterized.Parameters(name = "{0}")
+    public static List<FlagsParameterization> getFlags() {
+        return FlagsParameterization.allCombinationsOf(
+                Flags.FLAG_DELAYED_WAKELOCK_RELEASE_ON_BACKGROUND_THREAD);
+    }
+
+    @Rule public final SetFlagsRule mSetFlagsRule;
+
+    public WakeLockTest(FlagsParameterization flags) {
+        mSetFlagsRule = new SetFlagsRule(SetFlagsRule.DefaultInitValueType.NULL_DEFAULT, flags);
+    }
+
     private static final String WHY = "test";
     WakeLock mWakeLock;
     PowerManager.WakeLock mInner;
@@ -91,10 +110,7 @@
 
     @Test
     public void prodBuild_wakeLock_releaseWithoutAcquire_noThrow() {
-        if (Build.IS_ENG) {
-            return;
-        }
-
+        Assume.assumeFalse(Build.IS_ENG);
         // shouldn't throw an exception on production builds
         mWakeLock.release(WHY);
     }