diff --git a/osu.Desktop/Updater/VelopackUpdateManager.cs b/osu.Desktop/Updater/VelopackUpdateManager.cs
index 386a62d673..12a8b7a05d 100644
--- a/osu.Desktop/Updater/VelopackUpdateManager.cs
+++ b/osu.Desktop/Updater/VelopackUpdateManager.cs
@@ -37,7 +37,7 @@ namespace osu.Desktop.Updater
             scheduledBackgroundCheck = Scheduler.AddDelayed(() =>
             {
                 Logger.Log("Running scheduled background update check...");
-                Task.Run(CheckForUpdateAsync);
+                CheckForUpdate();
             }, 60000 * 30);
         }
 
@@ -60,6 +60,13 @@ namespace osu.Desktop.Updater
 
             UpdateInfo? update = await updateManager.CheckForUpdatesAsync().ConfigureAwait(false);
 
+            if (cancellationToken.IsCancellationRequested)
+            {
+                Logger.Log("Update check cancelled");
+                scheduleNextUpdateCheck();
+                return true;
+            }
+
             if (update == null)
             {
                 // No update is available.
@@ -68,9 +75,8 @@ namespace osu.Desktop.Updater
                 return false;
             }
 
-            Logger.Log($"New update available: {update.TargetFullRelease.Version}");
-
             // Download update in the background while notifying awaiters of the update being available.
+            Logger.Log($"New update available: {update.TargetFullRelease.Version}");
             downloadUpdate(updateManager, update, cancellationToken);
             return true;
         }
diff --git a/osu.Game/Overlays/Settings/Sections/General/UpdateSettings.cs b/osu.Game/Overlays/Settings/Sections/General/UpdateSettings.cs
index ac6215f3ad..b8a77a7688 100644
--- a/osu.Game/Overlays/Settings/Sections/General/UpdateSettings.cs
+++ b/osu.Game/Overlays/Settings/Sections/General/UpdateSettings.cs
@@ -126,7 +126,7 @@ namespace osu.Game.Overlays.Settings.Sections.General
 
             try
             {
-                bool foundUpdate = await updateManager.CheckForUpdateAsync().ConfigureAwait(true);
+                bool foundUpdate = await updateManager.CheckForUpdateAsync(checkingNotification.CancellationToken).ConfigureAwait(true);
 
                 if (!foundUpdate)
                 {
@@ -142,8 +142,9 @@ namespace osu.Game.Overlays.Settings.Sections.General
             }
             finally
             {
-                // This sequence allows the notification to be immediately dismissed.
-                checkingNotification.State = ProgressNotificationState.Cancelled;
+                // This sequence allows the notification to be immediately dismissed without posting a continuation message.
+                checkingNotification.CompletionTarget = null;
+                checkingNotification.State = ProgressNotificationState.Completed;
                 checkingNotification.Close(false);
                 checkForUpdatesButton.Enabled.Value = true;
             }
diff --git a/osu.Game/Updater/UpdateManager.cs b/osu.Game/Updater/UpdateManager.cs
index 3855ddd0d6..76557a4c77 100644
--- a/osu.Game/Updater/UpdateManager.cs
+++ b/osu.Game/Updater/UpdateManager.cs
@@ -44,6 +44,7 @@ namespace osu.Game.Updater
         protected IBindable<ReleaseStream> ReleaseStream => releaseStream;
 
         private readonly Bindable<ReleaseStream> releaseStream = new Bindable<ReleaseStream>();
+        private CancellationTokenSource updateCancellation = new CancellationTokenSource();
 
         protected override void LoadComplete()
         {
@@ -67,22 +68,35 @@ namespace osu.Game.Updater
             config.SetValue(OsuSetting.Version, version);
 
             config.BindWith(OsuSetting.ReleaseStream, releaseStream);
-            releaseStream.BindValueChanged(_ => CheckForUpdateAsync());
+            releaseStream.BindValueChanged(_ => CheckForUpdate());
 
-            CheckForUpdateAsync();
+            CheckForUpdate();
         }
 
-        private CancellationTokenSource? updateCheckCancellation;
+        /// <summary>
+        /// Immediately checks for any available update.
+        /// </summary>
+        public void CheckForUpdate()
+        {
+            _ = CheckForUpdateAsync();
+        }
 
         /// <summary>
-        /// Immediately checks for any available updates, or returns the existing update task.
+        /// Immediately checks for any available update.
         /// </summary>
         /// <returns><c>true</c> if any updates are available, <c>false</c> otherwise.</returns>
-        public Task<bool> CheckForUpdateAsync()
+        public async Task<bool> CheckForUpdateAsync(CancellationToken cancellationToken = default)
         {
-            updateCheckCancellation?.Cancel();
-            updateCheckCancellation = new CancellationTokenSource();
-            return PerformUpdateCheck(updateCheckCancellation.Token);
+            var cancellation = CancellationTokenSource.CreateLinkedTokenSource(cancellationToken);
+            var lastCancellation = Interlocked.Exchange(ref updateCancellation, cancellation);
+
+            using (lastCancellation)
+            {
+                // This serves a dual purpose of nullifying the last update, closing any existing notifications as stale.
+                await lastCancellation.CancelAsync().ConfigureAwait(false);
+            }
+
+            return await PerformUpdateCheck(cancellation.Token).ConfigureAwait(false);
         }
 
         /// <summary>
@@ -91,12 +105,6 @@ namespace osu.Game.Updater
         /// <returns>Whether any update is waiting. May return true if an error occured (there is potentially an update available).</returns>
         protected virtual Task<bool> PerformUpdateCheck(CancellationToken cancellationToken) => Task.FromResult(false);
 
-        protected override void Dispose(bool isDisposing)
-        {
-            base.Dispose(isDisposing);
-            updateCheckCancellation?.Cancel();
-        }
-
         private partial class UpdateCompleteNotification : SimpleNotification
         {
             private readonly string version;