diff --git a/src/Avalonia.Base/Platform/Storage/FallbackStorageProvider.cs b/src/Avalonia.Base/Platform/Storage/FallbackStorageProvider.cs
index 0192c6d38c..0852bbf329 100644
--- a/src/Avalonia.Base/Platform/Storage/FallbackStorageProvider.cs
+++ b/src/Avalonia.Base/Platform/Storage/FallbackStorageProvider.cs
@@ -8,7 +8,7 @@ namespace Avalonia.Platform.Storage;
 
 internal class FallbackStorageProvider : IStorageProvider
 {
-    private readonly Func<Task<IStorageProvider?>>[] _factories;
+    private Func<Task<IStorageProvider?>>[] _factories;
     private readonly List<IStorageProvider> _providers = new();
     private int _nextProviderFactory = 0;
     
@@ -16,6 +16,18 @@ internal class FallbackStorageProvider : IStorageProvider
     {
         _factories = factories;
     }
+
+    /// <summary>
+    /// Discards any cached providers and replaces the factory list. Useful when the
+    /// underlying platform state has changed (e.g. wayland compositor reconnect) and
+    /// previously-selected providers may no longer be appropriate.
+    /// </summary>
+    public void Reset(Func<Task<IStorageProvider?>>[] factories)
+    {
+        _factories = factories;
+        _providers.Clear();
+        _nextProviderFactory = 0;
+    }
     
     async IAsyncEnumerable<IStorageProvider> GetProviders()
     {
diff --git a/src/Avalonia.FreeDesktop/DBusSystemDialog.cs b/src/Avalonia.FreeDesktop/DBusSystemDialog.cs
index 1def2a4659..4434400475 100644
--- a/src/Avalonia.FreeDesktop/DBusSystemDialog.cs
+++ b/src/Avalonia.FreeDesktop/DBusSystemDialog.cs
@@ -16,7 +16,16 @@ namespace Avalonia.FreeDesktop
 {
     internal class DBusSystemDialog : BclStorageProvider
     {
-        internal static async Task<IStorageProvider?> TryCreateAsync(IPlatformHandle handle)
+        /// <summary>
+        /// Creates a portal-backed storage provider if xdg-desktop-portal FileChooser is available.
+        /// </summary>
+        /// <param name="parentLeaseProvider">
+        /// Callback invoked once per picker call to obtain the parent-window handle to pass to the
+        /// portal. The returned <see cref="IPortalParentLease"/> is held until the picker call
+        /// completes and then disposed. May return <c>null</c> to call the portal with an empty
+        /// parent_window string (per portal spec: "no parent").
+        /// </param>
+        internal static async Task<IStorageProvider?> TryCreateAsync(Func<Task<IPortalParentLease?>>? parentLeaseProvider)
         {
             if (DBusHelper.DefaultConnection is not { } conn)
                 return null;
@@ -35,23 +44,26 @@ namespace Avalonia.FreeDesktop
                 return null;
             }
 
-            return new DBusSystemDialog(conn, handle, dbusFileChooser, version);
+            return new DBusSystemDialog(conn, parentLeaseProvider, dbusFileChooser, version);
         }
 
         private readonly Connection _connection;
         private readonly OrgFreedesktopPortalFileChooserProxy _fileChooser;
-        private readonly IPlatformHandle _handle;
+        private readonly Func<Task<IPortalParentLease?>>? _parentLeaseProvider;
         private readonly uint _version;
 
-        private DBusSystemDialog(Connection connection, IPlatformHandle handle,
+        private DBusSystemDialog(Connection connection, Func<Task<IPortalParentLease?>>? parentLeaseProvider,
             OrgFreedesktopPortalFileChooserProxy fileChooser, uint version)
         {
             _connection = connection;
             _fileChooser = fileChooser;
-            _handle = handle;
+            _parentLeaseProvider = parentLeaseProvider;
             _version = version;
         }
 
+        private async Task<IPortalParentLease?> AcquireParentLeaseAsync()
+            => _parentLeaseProvider is null ? null : await _parentLeaseProvider().ConfigureAwait(false);
+
         public override bool CanOpen => true;
 
         public override bool CanSave => true;
@@ -60,7 +72,8 @@ namespace Avalonia.FreeDesktop
 
         public override async Task<IReadOnlyList<IStorageFile>> OpenFilePickerAsync(FilePickerOpenOptions options)
         {
-            var parentWindow = $"x11:{_handle.Handle:X}";
+            await using var parentLease = await AcquireParentLeaseAsync().ConfigureAwait(false);
+            var parentWindow = parentLease?.Handle ?? string.Empty;
             ObjectPath objectPath;
             var chooserOptions = new Dictionary<string, VariantValue>();
 
@@ -109,7 +122,8 @@ namespace Avalonia.FreeDesktop
         private async Task<(IStorageFile? file, FilePickerFileType? selectedType)> SaveFilePickerCoreAsync(
             FilePickerSaveOptions options)
         {
-            var parentWindow = $"x11:{_handle.Handle:X}";
+            await using var parentLease = await AcquireParentLeaseAsync().ConfigureAwait(false);
+            var parentWindow = parentLease?.Handle ?? string.Empty;
             ObjectPath objectPath;
             var chooserOptions = new Dictionary<string, VariantValue>();
             if (TryParseFilters(options.FileTypeChoices, options.SuggestedFileType, out var filters,
@@ -182,7 +196,8 @@ namespace Avalonia.FreeDesktop
             if (_version < 3)
                 return [];
 
-            var parentWindow = $"x11:{_handle.Handle:X}";
+            await using var parentLease = await AcquireParentLeaseAsync().ConfigureAwait(false);
+            var parentWindow = parentLease?.Handle ?? string.Empty;
             var chooserOptions = new Dictionary<string, VariantValue>
             {
                 { "directory", VariantValue.Bool(true) }, { "multiple", VariantValue.Bool(options.AllowMultiple) }
diff --git a/src/Avalonia.FreeDesktop/IPortalParentLease.cs b/src/Avalonia.FreeDesktop/IPortalParentLease.cs
new file mode 100644
index 0000000000..190070bd40
--- /dev/null
+++ b/src/Avalonia.FreeDesktop/IPortalParentLease.cs
@@ -0,0 +1,29 @@
+using System;
+using System.Threading.Tasks;
+
+namespace Avalonia.FreeDesktop;
+
+/// <summary>
+/// Backend-provided lease on a <c>parent_window</c> handle string suitable for passing
+/// to <c>org.freedesktop.portal.FileChooser</c> et al.
+/// </summary>
+/// <remarks>
+/// <para>The handle string is in the platform-prefixed format defined by xdg-desktop-portal:
+/// <c>x11:HEX</c> for X11, <c>wayland:HANDLE</c> for wayland.</para>
+/// <para>Disposal frees any platform resources backing the handle. For wayland this destroys
+/// the <c>zxdg_exported_v2</c> object that provided the handle string; the imported handle
+/// on the portal side becomes invalid afterwards, so the lease MUST be held until the
+/// portal call completes.</para>
+/// </remarks>
+internal interface IPortalParentLease : IAsyncDisposable
+{
+    /// <summary>Prefixed parent-window handle string (e.g. <c>"x11:1A2B"</c>).</summary>
+    string Handle { get; }
+}
+
+internal sealed class TrivialPortalParentLease : IPortalParentLease
+{
+    public TrivialPortalParentLease(string handle) => Handle = handle;
+    public string Handle { get; }
+    public ValueTask DisposeAsync() => default;
+}
diff --git a/src/Avalonia.X11/X11Window.cs b/src/Avalonia.X11/X11Window.cs
index 661c720f40..91fbfb93d2 100644
--- a/src/Avalonia.X11/X11Window.cs
+++ b/src/Avalonia.X11/X11Window.cs
@@ -269,7 +269,8 @@ namespace Avalonia.X11
             _storageProvider = new FallbackStorageProvider(new[]
             {
                 () => _platform.Options.UseDBusFilePicker
-                    ? DBusSystemDialog.TryCreateAsync(Handle)
+                    ? DBusSystemDialog.TryCreateAsync(() => Task.FromResult<IPortalParentLease?>(
+                        new TrivialPortalParentLease($"x11:{Handle.Handle:X}")))
                     : Task.FromResult<IStorageProvider?>(null),
                 () => GtkSystemDialog.TryCreate(this),
                 // TODO: This will be incompatible with "root element is not a TopLevel" scenarios,