diff --git a/src/cascadia/TerminalApp/TerminalPage.cpp b/src/cascadia/TerminalApp/TerminalPage.cpp
index fbbc8a4076..47dee8aae7 100644
--- a/src/cascadia/TerminalApp/TerminalPage.cpp
+++ b/src/cascadia/TerminalApp/TerminalPage.cpp
@@ -1069,7 +1069,7 @@ namespace winrt::TerminalApp::implementation
                 auto folderEntryItems = _CreateNewTabFlyoutItems(folderEntries);
 
                 // If the folder should auto-inline and there is only one item, do so.
-                if (folderEntry.Inlining() == FolderEntryInlining::Auto && folderEntries.Size() == 1)
+                if (folderEntry.Inlining() == FolderEntryInlining::Auto && folderEntryItems.size() == 1)
                 {
                     for (auto const& folderEntryItem : folderEntryItems)
                     {
diff --git a/src/cascadia/TerminalSettingsModel/ApplicationState.h b/src/cascadia/TerminalSettingsModel/ApplicationState.h
index 999ab0c0fc..f998fc5ead 100644
--- a/src/cascadia/TerminalSettingsModel/ApplicationState.h
+++ b/src/cascadia/TerminalSettingsModel/ApplicationState.h
@@ -41,7 +41,8 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
     X(FileSource::Shared, Windows::Foundation::Collections::IVector<hstring>, RecentCommands, "recentCommands")                                                           \
     X(FileSource::Shared, Windows::Foundation::Collections::IVector<winrt::Microsoft::Terminal::Settings::Model::InfoBarMessage>, DismissedMessages, "dismissedMessages") \
     X(FileSource::Local, Windows::Foundation::Collections::IVector<hstring>, AllowedCommandlines, "allowedCommandlines")                                                  \
-    X(FileSource::Local, std::unordered_set<hstring>, DismissedBadges, "dismissedBadges")
+    X(FileSource::Local, std::unordered_set<hstring>, DismissedBadges, "dismissedBadges")                                                                                 \
+    X(FileSource::Shared, bool, SSHFolderGenerated, "sshFolderGenerated", false)
 
     struct WindowLayout : WindowLayoutT<WindowLayout>
     {
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettings.h b/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
index 5e235d62af..8336db13f0 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
@@ -93,6 +93,7 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
         void MergeFragmentIntoUserSettings(const winrt::hstring& source, const winrt::hstring& basePath, const std::string_view& content);
         void FinalizeLayering();
         bool DisableDeletedProfiles();
+        bool AddDynamicProfileFolders();
         bool RemapColorSchemeForProfile(const winrt::com_ptr<winrt::Microsoft::Terminal::Settings::Model::implementation::Profile>& profile);
         bool FixupUserSettings();
 
@@ -100,6 +101,7 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
         ParsedSettings userSettings;
         std::unordered_map<hstring, winrt::com_ptr<implementation::ExtensionPackage>> extensionPackageMap;
         bool duplicateProfile = false;
+        bool sshProfilesGenerated = false;
 
     private:
         struct JsonSettings
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp b/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
index bb00ac550e..f251d3e027 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
@@ -213,8 +213,11 @@ void SettingsLoader::GenerateProfiles()
     auto generateProfiles = [&](const IDynamicProfileGenerator& generator) {
         if (!_ignoredNamespaces.contains(generator.GetNamespace()))
         {
+            const auto oldProfileCount = inboxSettings.profiles.size();
             _executeGenerator(generator, inboxSettings.profiles);
+            return oldProfileCount != inboxSettings.profiles.size();
         }
+        return false;
     };
 
     // Generate profiles for each generator and add them to the inbox settings.
@@ -224,7 +227,7 @@ void SettingsLoader::GenerateProfiles()
     generateProfiles(AzureCloudShellGenerator{});
     generateProfiles(VisualStudioGenerator{});
 #if TIL_FEATURE_DYNAMICSSHPROFILES_ENABLED
-    generateProfiles(SshHostGenerator{});
+    sshProfilesGenerated = generateProfiles(SshHostGenerator{});
 #endif
 }
 
@@ -536,6 +539,33 @@ bool SettingsLoader::DisableDeletedProfiles()
     return newGeneratedProfiles;
 }
 
+// Returns true if something got changed and
+// the settings need to be saved to disk.
+bool SettingsLoader::AddDynamicProfileFolders()
+{
+    // Keep track of generated folders to avoid regenerating them
+    const auto state = get_self<ApplicationState>(ApplicationState::SharedInstance());
+
+    // If the SSH generator is enabled, try to create an "SSH" folder with all the generated profiles
+    if (sshProfilesGenerated && !state->SSHFolderGenerated())
+    {
+        SshHostGenerator sshGenerator;
+        auto matchProfilesEntry = make_self<implementation::MatchProfilesEntry>();
+        matchProfilesEntry->Source(hstring{ sshGenerator.GetNamespace() });
+
+        auto folderEntry = make_self<implementation::FolderEntry>();
+        folderEntry->Name(L"SSH");
+        folderEntry->Icon(MediaResource::FromString(hstring{ sshGenerator.GetIcon() }));
+        folderEntry->Inlining(FolderEntryInlining::Auto);
+        folderEntry->RawEntries(winrt::single_threaded_vector<Model::NewTabMenuEntry>({ *matchProfilesEntry }));
+
+        userSettings.globals->NewTabMenu().Append(folderEntry.as<Model::NewTabMenuEntry>());
+        state->SSHFolderGenerated(true);
+        return true;
+    }
+    return false;
+}
+
 bool winrt::Microsoft::Terminal::Settings::Model::implementation::SettingsLoader::RemapColorSchemeForProfile(const winrt::com_ptr<winrt::Microsoft::Terminal::Settings::Model::implementation::Profile>& profile)
 {
     bool modified{ false };
@@ -1229,6 +1259,7 @@ try
     // DisableDeletedProfiles returns true whenever we encountered any new generated/dynamic profiles.
     // Similarly FixupUserSettings returns true, when it encountered settings that were patched up.
     mustWriteToDisk |= loader.DisableDeletedProfiles();
+    mustWriteToDisk |= loader.AddDynamicProfileFolders();
     mustWriteToDisk |= loader.FixupUserSettings();
 
     // If this throws, the app will catch it and use the default settings.