diff --git a/src/cascadia/TerminalSettingsEditor/Extensions.cpp b/src/cascadia/TerminalSettingsEditor/Extensions.cpp
index 1347c070d2f..1792785f93a 100644
--- a/src/cascadia/TerminalSettingsEditor/Extensions.cpp
+++ b/src/cascadia/TerminalSettingsEditor/Extensions.cpp
@@ -111,14 +111,25 @@ namespace winrt::Microsoft::Terminal::Settings::Editor::implementation
         _extensionSources.clear();
         _CurrentExtensionSource.clear();
 
-        std::vector<Editor::FragmentExtensionViewModel> fragmentExtensions;
-        fragmentExtensions.reserve(settings.FragmentExtensions().Size());
+        std::vector<Model::FragmentSettings> extensions;
+        extensions.reserve(settings.FragmentExtensions().Size() + settings.DynamicProfileGenerators().Size());
+        for (auto ext : settings.FragmentExtensions())
+        {
+            extensions.push_back(ext);
+        }
+        for (auto ext : settings.DynamicProfileGenerators())
+        {
+            extensions.push_back(ext);
+        }
+
+        std::vector<Editor::FragmentExtensionViewModel> extensionVMs;
+        extensionVMs.reserve(extensions.size());
 
         // these vectors track components all extensions successfully added
         std::vector<Editor::FragmentProfileViewModel> profilesModifiedTotal;
         std::vector<Editor::FragmentProfileViewModel> profilesAddedTotal;
         std::vector<Editor::FragmentColorSchemeViewModel> colorSchemesAddedTotal;
-        for (const auto&& fragExt : settings.FragmentExtensions())
+        for (const auto& fragExt : extensions)
         {
             const auto extensionEnabled = GetExtensionState(fragExt.Source());
 
@@ -173,10 +184,10 @@ namespace winrt::Microsoft::Terminal::Settings::Editor::implementation
             }
 
             _extensionSources.insert(fragExt.Source());
-            fragmentExtensions.push_back(winrt::make<FragmentExtensionViewModel>(fragExt, currentProfilesModified, currentProfilesAdded, currentColorSchemesAdded));
+            extensionVMs.push_back(winrt::make<FragmentExtensionViewModel>(fragExt, currentProfilesModified, currentProfilesAdded, currentColorSchemesAdded));
         }
 
-        _fragmentExtensions = single_threaded_observable_vector<Editor::FragmentExtensionViewModel>(std::move(fragmentExtensions));
+        _fragmentExtensions = single_threaded_observable_vector<Editor::FragmentExtensionViewModel>(std::move(extensionVMs));
         _profilesModifiedView = single_threaded_observable_vector<Editor::FragmentProfileViewModel>(std::move(profilesModifiedTotal));
         _profilesAddedView = single_threaded_observable_vector<Editor::FragmentProfileViewModel>(std::move(profilesAddedTotal));
         _colorSchemesAddedView = single_threaded_observable_vector<Editor::FragmentColorSchemeViewModel>(std::move(colorSchemesAddedTotal));
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettings.cpp b/src/cascadia/TerminalSettingsModel/CascadiaSettings.cpp
index 8d76d42dd65..c7a5f8d2928 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettings.cpp
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettings.cpp
@@ -124,6 +124,17 @@ Model::CascadiaSettings CascadiaSettings::Copy() const
             }
             settings->_fragmentExtensions = winrt::single_threaded_vector(std::move(fragmentExtensions));
         }
+
+        // copy dynamic profile generators
+        {
+            std::vector<Model::FragmentSettings> dynamicProfileGenerators;
+            dynamicProfileGenerators.reserve(_dynamicProfileGeneratorExtensions.Size());
+            for (const auto& fragment : _dynamicProfileGeneratorExtensions)
+            {
+                dynamicProfileGenerators.emplace_back(get_self<FragmentSettings>(fragment)->Copy());
+            }
+            settings->_dynamicProfileGeneratorExtensions = winrt::single_threaded_vector(std::move(dynamicProfileGenerators));
+        }
     }
 
     // load errors
@@ -220,6 +231,11 @@ IVectorView<Model::FragmentSettings> CascadiaSettings::FragmentExtensions() cons
     return _fragmentExtensions.GetView();
 }
 
+IVectorView<Model::FragmentSettings> CascadiaSettings::DynamicProfileGenerators() const noexcept
+{
+    return _dynamicProfileGeneratorExtensions.GetView();
+}
+
 // Method Description:
 // - Returns the globally configured keybindings
 // Arguments:
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettings.h b/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
index f772303cbc8..22238092bb7 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettings.h
@@ -74,6 +74,7 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
         ParsedSettings inboxSettings;
         ParsedSettings userSettings;
         std::vector<Model::FragmentSettings> fragmentExtensions;
+        std::vector<Model::FragmentSettings> dynamicProfileGeneratorExtensions;
         bool duplicateProfile = false;
 
     private:
@@ -132,6 +133,7 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
         winrt::Windows::Foundation::Collections::IObservableVector<Model::Profile> ActiveProfiles() const noexcept;
         Model::ActionMap ActionMap() const noexcept;
         winrt::Windows::Foundation::Collections::IVectorView<Model::FragmentSettings> FragmentExtensions() const noexcept;
+        winrt::Windows::Foundation::Collections::IVectorView<Model::FragmentSettings> DynamicProfileGenerators() const noexcept;
         void WriteSettingsToDisk();
         Json::Value ToJson() const;
         Model::Profile ProfileDefaults() const;
@@ -190,6 +192,7 @@ namespace winrt::Microsoft::Terminal::Settings::Model::implementation
         winrt::Windows::Foundation::Collections::IObservableVector<Model::Profile> _allProfiles = winrt::single_threaded_observable_vector<Model::Profile>();
         winrt::Windows::Foundation::Collections::IObservableVector<Model::Profile> _activeProfiles = winrt::single_threaded_observable_vector<Model::Profile>();
         winrt::Windows::Foundation::Collections::IVector<Model::FragmentSettings> _fragmentExtensions = winrt::single_threaded_vector<Model::FragmentSettings>();
+        winrt::Windows::Foundation::Collections::IVector<Model::FragmentSettings> _dynamicProfileGeneratorExtensions = winrt::single_threaded_vector<Model::FragmentSettings>();
         std::set<std::string> _themesChangeLog{};
 
         // load errors
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettings.idl b/src/cascadia/TerminalSettingsModel/CascadiaSettings.idl
index 25b65e1ad18..5671ed21d42 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettings.idl
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettings.idl
@@ -45,6 +45,7 @@ namespace Microsoft.Terminal.Settings.Model
 
         ActionMap ActionMap { get; };
         Windows.Foundation.Collections.IVectorView<FragmentSettings> FragmentExtensions { get; };
+        Windows.Foundation.Collections.IVectorView<FragmentSettings> DynamicProfileGenerators { get; };
 
         IVectorView<SettingsLoadWarnings> Warnings { get; };
         Windows.Foundation.IReference<SettingsLoadErrors> GetLoadingError { get; };
diff --git a/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp b/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
index 0997a37a966..9ec727253a8 100644
--- a/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
+++ b/src/cascadia/TerminalSettingsModel/CascadiaSettingsSerialization.cpp
@@ -991,31 +991,51 @@ bool SettingsLoader::_addOrMergeUserColorScheme(const winrt::com_ptr<implementat
 void SettingsLoader::_executeGenerator(const IDynamicProfileGenerator& generator)
 {
     const auto generatorNamespace = generator.GetNamespace();
-    if (_ignoredNamespaces.contains(generatorNamespace))
-    {
-        return;
-    }
-
-    const auto previousSize = inboxSettings.profiles.size();
-
+    std::vector<winrt::com_ptr<implementation::Profile>> generatedProfiles;
     try
     {
-        generator.GenerateProfiles(inboxSettings.profiles);
+        generator.GenerateProfiles(generatedProfiles);
     }
     CATCH_LOG_MSG("Dynamic Profile Namespace: \"%.*s\"", gsl::narrow<int>(generatorNamespace.size()), generatorNamespace.data())
 
+    // These are needed for the FragmentSettings object
+    std::vector<Model::FragmentProfileEntry> profileEntries;
+    Json::Value profilesListJson{ Json::ValueType::arrayValue };
+    Json::StreamWriterBuilder styledWriter;
+    styledWriter["indentation"] = "    ";
+
     // If the generator produced some profiles we're going to give them default attributes.
     // By setting the Origin/Source/etc. here, we deduplicate some code and ensure they aren't missing accidentally.
-    if (inboxSettings.profiles.size() > previousSize)
+    const winrt::hstring source{ generatorNamespace };
+    for (const auto& profile : generatedProfiles)
     {
-        const winrt::hstring source{ generatorNamespace };
+        profile->Origin(OriginTag::Generated);
+        profile->Source(source);
+
+        const auto profileJson = profile->ToJson();
+        profilesListJson.append(profileJson);
+        profileEntries.push_back(winrt::make<FragmentProfileEntry>(profile->Guid(), hstring{ til::u8u16(Json::writeString(styledWriter, profileJson)) }));
+    }
 
-        for (const auto& profile : std::span(inboxSettings.profiles).subspan(previousSize))
+    if (!_ignoredNamespaces.contains(generatorNamespace))
+    {
+        // Add generated profiles to the user settings
+        for (auto& profile : generatedProfiles)
         {
-            profile->Origin(OriginTag::Generated);
-            profile->Source(source);
+            inboxSettings.profiles.push_back(profile);
         }
     }
+
+    // Manually construct the JSON for the FragmentSettings object
+    Json::Value json{ Json::ValueType::objectValue };
+    json[JsonKey(ProfilesKey)] = profilesListJson;
+
+    auto generatorExtension = winrt::make_self<FragmentSettings>(hstring{ generatorNamespace }, hstring{ til::u8u16(Json::writeString(styledWriter, json)) }, hstring{ L"settings.json" }, FragmentScope::Machine);
+    for (const auto& entry : profileEntries)
+    {
+        generatorExtension->NewProfiles().Append(entry);
+    }
+    dynamicProfileGeneratorExtensions.emplace_back(*generatorExtension);
 }
 
 // Method Description:
@@ -1308,6 +1328,7 @@ CascadiaSettings::CascadiaSettings(SettingsLoader&& loader) :
     _warnings = winrt::single_threaded_vector(std::move(warnings));
     _themesChangeLog = std::move(loader.userSettings.themesChangeLog);
     _fragmentExtensions = winrt::single_threaded_vector(std::move(loader.fragmentExtensions));
+    _dynamicProfileGeneratorExtensions = winrt::single_threaded_vector(std::move(loader.dynamicProfileGeneratorExtensions));
 
     _resolveDefaultProfile();
     _resolveNewTabMenuProfiles();