diff --git a/src/Ryujinx.UI.Common/Configuration/ConfigurationFileFormat.cs b/src/Ryujinx.UI.Common/Configuration/ConfigurationFileFormat.cs
index e60fac09bf..2ccb67c70a 100644
--- a/src/Ryujinx.UI.Common/Configuration/ConfigurationFileFormat.cs
+++ b/src/Ryujinx.UI.Common/Configuration/ConfigurationFileFormat.cs
@@ -15,7 +15,7 @@ namespace Ryujinx.UI.Common.Configuration
         /// <summary>
         /// The current version of the file format
         /// </summary>
-        public const int CurrentVersion = 52;
+        public const int CurrentVersion = 53;
 
         /// <summary>
         /// Version of the configuration file format
@@ -266,6 +266,11 @@ namespace Ryujinx.UI.Common.Configuration
         /// A list of directories containing games to be used to load games into the games list
         /// </summary>
         public List<string> GameDirs { get; set; }
+        
+        /// <summary>
+        /// A list of directories containing DLC/updates the user wants to autoload during library refreshes
+        /// </summary>
+        public List<string> AutoloadDirs { get; set; }
 
         /// <summary>
         /// A list of file types to be hidden in the games List
diff --git a/src/Ryujinx.UI.Common/Configuration/ConfigurationState.cs b/src/Ryujinx.UI.Common/Configuration/ConfigurationState.cs
index 4cd85aa01b..f9179d0c07 100644
--- a/src/Ryujinx.UI.Common/Configuration/ConfigurationState.cs
+++ b/src/Ryujinx.UI.Common/Configuration/ConfigurationState.cs
@@ -121,6 +121,11 @@ namespace Ryujinx.UI.Common.Configuration
             /// A list of directories containing games to be used to load games into the games list
             /// </summary>
             public ReactiveObject<List<string>> GameDirs { get; private set; }
+            
+            /// <summary>
+            /// A list of directories containing DLC/updates the user wants to autoload during library refreshes
+            /// </summary>
+            public ReactiveObject<List<string>> AutoloadDirs { get; private set; }
 
             /// <summary>
             /// A list of file types to be hidden in the games List
@@ -192,6 +197,7 @@ namespace Ryujinx.UI.Common.Configuration
                 GuiColumns = new Columns();
                 ColumnSort = new ColumnSortSettings();
                 GameDirs = new ReactiveObject<List<string>>();
+                AutoloadDirs = new ReactiveObject<List<string>>();
                 ShownFileTypes = new ShownFileTypeSettings();
                 WindowStartup = new WindowStartupSettings();
                 EnableCustomTheme = new ReactiveObject<bool>();
@@ -735,6 +741,7 @@ namespace Ryujinx.UI.Common.Configuration
                     SortAscending = UI.ColumnSort.SortAscending,
                 },
                 GameDirs = UI.GameDirs,
+                AutoloadDirs = UI.AutoloadDirs,
                 ShownFileTypes = new ShownFileTypes
                 {
                     NSP = UI.ShownFileTypes.NSP,
@@ -844,6 +851,7 @@ namespace Ryujinx.UI.Common.Configuration
             UI.ColumnSort.SortColumnId.Value = 0;
             UI.ColumnSort.SortAscending.Value = false;
             UI.GameDirs.Value = new List<string>();
+            UI.AutoloadDirs.Value = new List<string>();
             UI.ShownFileTypes.NSP.Value = true;
             UI.ShownFileTypes.PFS0.Value = true;
             UI.ShownFileTypes.XCI.Value = true;
@@ -1493,6 +1501,15 @@ namespace Ryujinx.UI.Common.Configuration
 
                 configurationFileUpdated = true;
             }
+            
+            if (configurationFileFormat.Version < 53)
+            {
+                Ryujinx.Common.Logging.Logger.Warning?.Print(LogClass.Application, $"Outdated configuration version {configurationFileFormat.Version}, migrating to version 53.");
+
+                configurationFileFormat.AutoloadDirs = new();
+
+                configurationFileUpdated = true;
+            }
 
             Logger.EnableFileLog.Value = configurationFileFormat.EnableFileLog;
             Graphics.ResScale.Value = configurationFileFormat.ResScale;
@@ -1556,6 +1573,7 @@ namespace Ryujinx.UI.Common.Configuration
             UI.ColumnSort.SortColumnId.Value = configurationFileFormat.ColumnSort.SortColumnId;
             UI.ColumnSort.SortAscending.Value = configurationFileFormat.ColumnSort.SortAscending;
             UI.GameDirs.Value = configurationFileFormat.GameDirs;
+            UI.AutoloadDirs.Value = configurationFileFormat.AutoloadDirs;
             UI.ShownFileTypes.NSP.Value = configurationFileFormat.ShownFileTypes.NSP;
             UI.ShownFileTypes.PFS0.Value = configurationFileFormat.ShownFileTypes.PFS0;
             UI.ShownFileTypes.XCI.Value = configurationFileFormat.ShownFileTypes.XCI;
diff --git a/src/Ryujinx/Assets/Locales/en_US.json b/src/Ryujinx/Assets/Locales/en_US.json
index 6f050ec1b3..339842616e 100644
--- a/src/Ryujinx/Assets/Locales/en_US.json
+++ b/src/Ryujinx/Assets/Locales/en_US.json
@@ -106,6 +106,7 @@
   "SettingsTabGeneralHideCursorOnIdle": "On Idle",
   "SettingsTabGeneralHideCursorAlways": "Always",
   "SettingsTabGeneralGameDirectories": "Game Directories",
+  "SettingsTabGeneralAutoloadDirectories": "Autoload DLC/Updates Directories",
   "SettingsTabGeneralAdd": "Add",
   "SettingsTabGeneralRemove": "Remove",
   "SettingsTabSystem": "System",
@@ -559,6 +560,9 @@
   "AddGameDirBoxTooltip": "Enter a game directory to add to the list",
   "AddGameDirTooltip": "Add a game directory to the list",
   "RemoveGameDirTooltip": "Remove selected game directory",
+  "AddAutoloadDirBoxTooltip": "Enter an autoload directory to add to the list",
+  "AddAutoloadDirTooltip": "Add an autoload directory to the list",
+  "RemoveAutoloadDirTooltip": "Remove selected autoload directory",
   "CustomThemeCheckTooltip": "Use a custom Avalonia theme for the GUI to change the appearance of the emulator menus",
   "CustomThemePathTooltip": "Path to custom GUI theme",
   "CustomThemeBrowseTooltip": "Browse for a custom GUI theme",
diff --git a/src/Ryujinx/UI/ViewModels/SettingsViewModel.cs b/src/Ryujinx/UI/ViewModels/SettingsViewModel.cs
index 9223e578d1..57c576e1fd 100644
--- a/src/Ryujinx/UI/ViewModels/SettingsViewModel.cs
+++ b/src/Ryujinx/UI/ViewModels/SettingsViewModel.cs
@@ -44,7 +44,8 @@ namespace Ryujinx.Ava.UI.ViewModels
         private int _graphicsBackendMultithreadingIndex;
         private float _volume;
         private bool _isVulkanAvailable = true;
-        private bool _directoryChanged;
+        private bool _gameDirectoryChanged;
+        private bool _autoloadDirectoryChanged;
         private readonly List<string> _gpuIds = new();
         private int _graphicsBackendIndex;
         private int _scalingFilter;
@@ -115,12 +116,23 @@ namespace Ryujinx.Ava.UI.ViewModels
 
         public bool IsHypervisorAvailable => OperatingSystem.IsMacOS() && RuntimeInformation.ProcessArchitecture == Architecture.Arm64;
 
-        public bool DirectoryChanged
+        public bool GameDirectoryChanged
         {
-            get => _directoryChanged;
+            get => _gameDirectoryChanged;
             set
             {
-                _directoryChanged = value;
+                _gameDirectoryChanged = value;
+
+                OnPropertyChanged();
+            }
+        }
+        
+        public bool AutoloadDirectoryChanged
+        {
+            get => _autoloadDirectoryChanged;
+            set
+            {
+                _autoloadDirectoryChanged = value;
 
                 OnPropertyChanged();
             }
@@ -231,6 +243,7 @@ namespace Ryujinx.Ava.UI.ViewModels
 
         internal AvaloniaList<TimeZone> TimeZones { get; set; }
         public AvaloniaList<string> GameDirectories { get; set; }
+        public AvaloniaList<string> AutoloadDirectories { get; set; }
         public ObservableCollection<ComboBoxItem> AvailableGpus { get; set; }
 
         public AvaloniaList<string> NetworkInterfaceList
@@ -273,6 +286,7 @@ namespace Ryujinx.Ava.UI.ViewModels
         public SettingsViewModel()
         {
             GameDirectories = new AvaloniaList<string>();
+            AutoloadDirectories = new AvaloniaList<string>();
             TimeZones = new AvaloniaList<TimeZone>();
             AvailableGpus = new ObservableCollection<ComboBoxItem>();
             _validTzRegions = new List<string>();
@@ -398,6 +412,9 @@ namespace Ryujinx.Ava.UI.ViewModels
 
             GameDirectories.Clear();
             GameDirectories.AddRange(config.UI.GameDirs.Value);
+            
+            AutoloadDirectories.Clear();
+            AutoloadDirectories.AddRange(config.UI.AutoloadDirs.Value);
 
             BaseStyleIndex = config.UI.BaseStyle.Value switch
             {
@@ -489,11 +506,17 @@ namespace Ryujinx.Ava.UI.ViewModels
             config.AutoloadContent.Value = AutoloadContent;
             config.HideCursor.Value = (HideCursorMode)HideCursor;
 
-            if (_directoryChanged)
+            if (_gameDirectoryChanged)
             {
                 List<string> gameDirs = new(GameDirectories);
                 config.UI.GameDirs.Value = gameDirs;
             }
+            
+            if (_autoloadDirectoryChanged)
+            {
+                List<string> autoloadDirs = new(AutoloadDirectories);
+                config.UI.AutoloadDirs.Value = autoloadDirs;
+            }
 
             config.UI.BaseStyle.Value = BaseStyleIndex switch
             {
@@ -590,7 +613,8 @@ namespace Ryujinx.Ava.UI.ViewModels
 
             SaveSettingsEvent?.Invoke();
 
-            _directoryChanged = false;
+            _gameDirectoryChanged = false;
+            _autoloadDirectoryChanged = false;
         }
 
         private static void RevertIfNotSaved()
diff --git a/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml b/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml
index 9d26effcc5..4f25cbebfb 100644
--- a/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml
+++ b/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml
@@ -88,7 +88,7 @@
                     Orientation="Vertical"
                     Spacing="10">
                     <ListBox
-                        Name="GameList"
+                        Name="GameDirsList"
                         MinHeight="230"
                         ItemsSource="{Binding GameDirectories}">
                         <ListBox.Styles>
@@ -105,27 +105,78 @@
                             <ColumnDefinition Width="Auto" />
                         </Grid.ColumnDefinitions>
                         <TextBox
-                            Name="PathBox"
+                            Name="GameDirPathBox"
                             Margin="0"
                             ToolTip.Tip="{locale:Locale AddGameDirBoxTooltip}"
                             VerticalAlignment="Stretch" />
                         <Button
-                            Name="AddButton"
+                            Name="AddGameDirButton"
                             Grid.Column="1"
                             MinWidth="90"
                             Margin="10,0,0,0"
                             ToolTip.Tip="{locale:Locale AddGameDirTooltip}"
-                            Click="AddButton_OnClick">
+                            Click="AddGameDirButton_OnClick">
                             <TextBlock HorizontalAlignment="Center"
                                        Text="{locale:Locale SettingsTabGeneralAdd}" />
                         </Button>
                         <Button
-                            Name="RemoveButton"
+                            Name="RemoveGameDirButton"
                             Grid.Column="2"
                             MinWidth="90"
                             Margin="10,0,0,0"
                             ToolTip.Tip="{locale:Locale RemoveGameDirTooltip}"
-                            Click="RemoveButton_OnClick">
+                            Click="RemoveGameDirButton_OnClick">
+                            <TextBlock HorizontalAlignment="Center"
+                                       Text="{locale:Locale SettingsTabGeneralRemove}" />
+                        </Button>
+                    </Grid>
+                </StackPanel>
+                <Separator Height="1" />
+                <TextBlock Classes="h1" Text="{locale:Locale SettingsTabGeneralAutoloadDirectories}" />
+                <StackPanel
+                    Margin="10,0,0,0"
+                    HorizontalAlignment="Stretch"
+                    Orientation="Vertical"
+                    Spacing="10">
+                    <ListBox
+                        Name="AutoloadDirsList"
+                        MinHeight="230"
+                        ItemsSource="{Binding AutoloadDirectories}">
+                        <ListBox.Styles>
+                            <Style Selector="ListBoxItem">
+                                <Setter Property="Padding" Value="10" />
+                                <Setter Property="Background" Value="{DynamicResource ListBoxBackground}" />
+                            </Style>
+                        </ListBox.Styles>
+                    </ListBox>
+                    <Grid HorizontalAlignment="Stretch">
+                        <Grid.ColumnDefinitions>
+                            <ColumnDefinition Width="*" />
+                            <ColumnDefinition Width="Auto" />
+                            <ColumnDefinition Width="Auto" />
+                        </Grid.ColumnDefinitions>
+                        <TextBox
+                            Name="AutoloadDirPathBox"
+                            Margin="0"
+                            ToolTip.Tip="{locale:Locale AddAutoloadDirBoxTooltip}"
+                            VerticalAlignment="Stretch" />
+                        <Button
+                            Name="AddAutoloadDirButton"
+                            Grid.Column="1"
+                            MinWidth="90"
+                            Margin="10,0,0,0"
+                            ToolTip.Tip="{locale:Locale AddAutoloadDirTooltip}"
+                            Click="AddAutoloadDirButton_OnClick">
+                            <TextBlock HorizontalAlignment="Center"
+                                       Text="{locale:Locale SettingsTabGeneralAdd}" />
+                        </Button>
+                        <Button
+                            Name="RemoveAutoloadDirButton"
+                            Grid.Column="2"
+                            MinWidth="90"
+                            Margin="10,0,0,0"
+                            ToolTip.Tip="{locale:Locale RemoveAutoloadDirTooltip}"
+                            Click="RemoveAutoloadDirButton_OnClick">
                             <TextBlock HorizontalAlignment="Center"
                                        Text="{locale:Locale SettingsTabGeneralRemove}" />
                         </Button>
diff --git a/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml.cs b/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml.cs
index 996d15cdbd..70ca323068 100644
--- a/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml.cs
+++ b/src/Ryujinx/UI/Views/Settings/SettingsUIView.axaml.cs
@@ -19,14 +19,14 @@ namespace Ryujinx.Ava.UI.Views.Settings
             InitializeComponent();
         }
 
-        private async void AddButton_OnClick(object sender, RoutedEventArgs e)
+        private async void AddGameDirButton_OnClick(object sender, RoutedEventArgs e)
         {
-            string path = PathBox.Text;
+            string path = GameDirPathBox.Text;
 
             if (!string.IsNullOrWhiteSpace(path) && Directory.Exists(path) && !ViewModel.GameDirectories.Contains(path))
             {
                 ViewModel.GameDirectories.Add(path);
-                ViewModel.DirectoryChanged = true;
+                ViewModel.GameDirectoryChanged = true;
             }
             else
             {
@@ -40,25 +40,68 @@ namespace Ryujinx.Ava.UI.Views.Settings
                     if (result.Count > 0)
                     {
                         ViewModel.GameDirectories.Add(result[0].Path.LocalPath);
-                        ViewModel.DirectoryChanged = true;
+                        ViewModel.GameDirectoryChanged = true;
                     }
                 }
             }
         }
 
-        private void RemoveButton_OnClick(object sender, RoutedEventArgs e)
+        private void RemoveGameDirButton_OnClick(object sender, RoutedEventArgs e)
         {
-            int oldIndex = GameList.SelectedIndex;
+            int oldIndex = GameDirsList.SelectedIndex;
 
-            foreach (string path in new List<string>(GameList.SelectedItems.Cast<string>()))
+            foreach (string path in new List<string>(GameDirsList.SelectedItems.Cast<string>()))
             {
                 ViewModel.GameDirectories.Remove(path);
-                ViewModel.DirectoryChanged = true;
+                ViewModel.GameDirectoryChanged = true;
             }
 
-            if (GameList.ItemCount > 0)
+            if (GameDirsList.ItemCount > 0)
             {
-                GameList.SelectedIndex = oldIndex < GameList.ItemCount ? oldIndex : 0;
+                GameDirsList.SelectedIndex = oldIndex < GameDirsList.ItemCount ? oldIndex : 0;
+            }
+        }
+        
+        private async void AddAutoloadDirButton_OnClick(object sender, RoutedEventArgs e)
+        {
+            string path = AutoloadDirPathBox.Text;
+
+            if (!string.IsNullOrWhiteSpace(path) && Directory.Exists(path) && !ViewModel.AutoloadDirectories.Contains(path))
+            {
+                ViewModel.AutoloadDirectories.Add(path);
+                ViewModel.AutoloadDirectoryChanged = true;
+            }
+            else
+            {
+                if (this.GetVisualRoot() is Window window)
+                {
+                    var result = await window.StorageProvider.OpenFolderPickerAsync(new FolderPickerOpenOptions
+                    {
+                        AllowMultiple = false,
+                    });
+
+                    if (result.Count > 0)
+                    {
+                        ViewModel.AutoloadDirectories.Add(result[0].Path.LocalPath);
+                        ViewModel.AutoloadDirectoryChanged = true;
+                    }
+                }
+            }
+        }
+
+        private void RemoveAutoloadDirButton_OnClick(object sender, RoutedEventArgs e)
+        {
+            int oldIndex = AutoloadDirsList.SelectedIndex;
+
+            foreach (string path in new List<string>(AutoloadDirsList.SelectedItems.Cast<string>()))
+            {
+                ViewModel.AutoloadDirectories.Remove(path);
+                ViewModel.AutoloadDirectoryChanged = true;
+            }
+
+            if (AutoloadDirsList.ItemCount > 0)
+            {
+                AutoloadDirsList.SelectedIndex = oldIndex < AutoloadDirsList.ItemCount ? oldIndex : 0;
             }
         }
     }
diff --git a/src/Ryujinx/UI/Windows/MainWindow.axaml.cs b/src/Ryujinx/UI/Windows/MainWindow.axaml.cs
index 7947b4896b..3b471fee82 100644
--- a/src/Ryujinx/UI/Windows/MainWindow.axaml.cs
+++ b/src/Ryujinx/UI/Windows/MainWindow.axaml.cs
@@ -642,17 +642,18 @@ namespace Ryujinx.Ava.UI.Windows
                 TimeIt("updates", () => ApplicationLibrary.LoadTitleUpdates());
                 TimeIt("DLC", () => ApplicationLibrary.LoadDownloadableContents());
 
-                if (ConfigurationState.Instance.AutoloadContent)
+                var autoloadDirs = ConfigurationState.Instance.UI.AutoloadDirs.Value;
+                if (autoloadDirs.Count > 0)
                 {
                     var updatesLoaded = 0;
                     TimeIt("auto updates",
                         () => updatesLoaded =
-                            ApplicationLibrary.AutoLoadTitleUpdates(ConfigurationState.Instance.UI.GameDirs));
+                            ApplicationLibrary.AutoLoadTitleUpdates(autoloadDirs));
 
                     var dlcLoaded = 0;
                     TimeIt("auto dlc",
                         () => dlcLoaded =
-                            ApplicationLibrary.AutoLoadDownloadableContents(ConfigurationState.Instance.UI.GameDirs));
+                            ApplicationLibrary.AutoLoadDownloadableContents(autoloadDirs));
 
                     ShowNewContentAddedDialog(dlcLoaded, updatesLoaded);
                 }
diff --git a/src/Ryujinx/UI/Windows/SettingsWindow.axaml.cs b/src/Ryujinx/UI/Windows/SettingsWindow.axaml.cs
index 314501c525..4d78718861 100644
--- a/src/Ryujinx/UI/Windows/SettingsWindow.axaml.cs
+++ b/src/Ryujinx/UI/Windows/SettingsWindow.axaml.cs
@@ -39,7 +39,7 @@ namespace Ryujinx.Ava.UI.Windows
         {
             InputPage.InputView?.SaveCurrentProfile();
 
-            if (Owner is MainWindow window && ViewModel.DirectoryChanged)
+            if (Owner is MainWindow window && (ViewModel.GameDirectoryChanged || ViewModel.AutoloadDirectoryChanged))
             {
                 window.LoadApplications();
             }