diff --git a/src/tribler/core/restapi/settings_endpoint.py b/src/tribler/core/restapi/settings_endpoint.py
index e5df86097c..65d0849357 100644
--- a/src/tribler/core/restapi/settings_endpoint.py
+++ b/src/tribler/core/restapi/settings_endpoint.py
@@ -69,9 +69,16 @@ async def update_settings(self, request: web.Request) -> RESTResponse:
 
         return RESTResponse({"modified": True})
 
-    def _recursive_merge_settings(self, existing: dict, updates: dict) -> None:
+    def _recursive_merge_settings(self, existing: dict, updates: dict, top: bool = True) -> None:
         for key in existing:
+            # Ignore top-level ui entry
+            if top and key == "ui":
+                continue
             value = updates.get(key, existing[key])
             if isinstance(value, dict):
-                self._recursive_merge_settings(existing[key], value)
+                self._recursive_merge_settings(existing[key], value, False)
             existing[key] = value
+
+        # Since the core doesn't need to be aware of the GUI settings, we just copy them.
+        if top and "ui" in updates:
+            existing["ui"].update(updates["ui"])
diff --git a/src/tribler/tribler_config.py b/src/tribler/tribler_config.py
index 27b0e2b3e4..99b9fd9097 100644
--- a/src/tribler/tribler_config.py
+++ b/src/tribler/tribler_config.py
@@ -27,6 +27,8 @@ class ApiConfig(TypedDict):
     https_enabled: bool
     https_host: str
     https_port: int
+    http_port_running: int
+    https_port_running: int
 
 
 class ContentDiscoveryCommunityConfig(TypedDict):
diff --git a/src/tribler/ui/src/components/add-torrent.tsx b/src/tribler/ui/src/components/add-torrent.tsx
index 7609d83ddd..081a83546b 100644
--- a/src/tribler/ui/src/components/add-torrent.tsx
+++ b/src/tribler/ui/src/components/add-torrent.tsx
@@ -124,7 +124,7 @@ export function AddTorrent() {
                     const files = Array.from(event.target.files as ArrayLike<File>);
                     event.target.value = '';
 
-                    if (files.length === 1 && triblerService.getGuiSettings().ask_download_settings !== false) {
+                    if (files.length === 1 && triblerService.guiSettings.ask_download_settings !== false) {
                         setSaveAsDialogOpen(true);
                         setTorrent(files[0]);
                     }
diff --git a/src/tribler/ui/src/components/language-select.tsx b/src/tribler/ui/src/components/language-select.tsx
index 37932c9f54..19fcef265b 100644
--- a/src/tribler/ui/src/components/language-select.tsx
+++ b/src/tribler/ui/src/components/language-select.tsx
@@ -3,18 +3,24 @@ import { Button } from "./ui/button";
 import { DropdownMenu, DropdownMenuContent, DropdownMenuItem, DropdownMenuTrigger } from "./ui/dropdown-menu";
 import { useTranslation } from "react-i18next";
 import { triblerService } from "@/services/tribler.service";
+import { useEffect } from "react";
 
 
 const LanguageSelect = () => {
     const { language, setLanguage } = useLanguage();
     const { t, i18n } = useTranslation();
 
-    const changeLanguage = (lng: string) => {
+    useEffect(() => {
+        const lng = triblerService.guiSettings.lang ?? 'en_US';
         setLanguage(lng);
         i18n.changeLanguage(lng);
-        triblerService.setGuiSettings({
-            ...triblerService.getGuiSettings(),
-            lang: lng
+    }, []);
+
+    const changeLanguage = async (lng: string) => {
+        setLanguage(lng);
+        i18n.changeLanguage(lng);
+        await triblerService.setSettings({
+            ui: { lang: lng }
         });
     };
 
diff --git a/src/tribler/ui/src/config/menu.ts b/src/tribler/ui/src/config/menu.ts
index 4b354337f5..75098d794a 100644
--- a/src/tribler/ui/src/config/menu.ts
+++ b/src/tribler/ui/src/config/menu.ts
@@ -89,7 +89,7 @@ export const sideMenu: NavItemWithChildren[] = [
     {
         title: 'Debug',
         icon: ExclamationTriangleIcon,
-        hide: () => triblerService.getGuiSettings().dev_mode !== true,
+        hide: () => triblerService.guiSettings.dev_mode !== true,
         items: [
             {
                 title: 'General',
diff --git a/src/tribler/ui/src/contexts/LanguageContext.tsx b/src/tribler/ui/src/contexts/LanguageContext.tsx
index 5ccb065c9a..75b2136290 100644
--- a/src/tribler/ui/src/contexts/LanguageContext.tsx
+++ b/src/tribler/ui/src/contexts/LanguageContext.tsx
@@ -9,7 +9,7 @@ interface LanguageContextType {
 const LanguageContext = createContext<LanguageContextType | undefined>(undefined);
 
 export const LanguageProvider: React.FC<React.PropsWithChildren> = ({ children }) => {
-    const [language, setLanguage] = useState(triblerService.getGuiSettings().lang ?? 'en');
+    const [language, setLanguage] = useState(triblerService.guiSettings.lang ?? 'en_US');
 
     return (
         <LanguageContext.Provider value={{ language, setLanguage }}>
diff --git a/src/tribler/ui/src/dialogs/SaveAs.tsx b/src/tribler/ui/src/dialogs/SaveAs.tsx
index f21f296430..ad7bba55d2 100644
--- a/src/tribler/ui/src/dialogs/SaveAs.tsx
+++ b/src/tribler/ui/src/dialogs/SaveAs.tsx
@@ -157,7 +157,7 @@ export default function SaveAs(props: SaveAsProps & JSX.IntrinsicAttributes & Di
         }
     }
 
-    if (props.open && props.onOpenChange && !triblerService.getGuiSettings().ask_download_settings) {
+    if (props.open && props.onOpenChange && triblerService.guiSettings.ask_download_settings === false) {
         OnDownloadClicked();
         return <></>;
     }
diff --git a/src/tribler/ui/src/i18n/index.ts b/src/tribler/ui/src/i18n/index.ts
index 77cfb3f0fa..37130117ac 100644
--- a/src/tribler/ui/src/i18n/index.ts
+++ b/src/tribler/ui/src/i18n/index.ts
@@ -8,7 +8,7 @@ i18n
     .use(initReactI18next)
     .init({
         supportedLngs: ['en_US', 'es_ES', 'pt_BR', 'ru_RU', 'zh_CN'],
-        lng: triblerService.getGuiSettings().lang,
+        lng: triblerService.guiSettings.lang,
         fallbackLng: 'en_US',
         interpolation: {
             escapeValue: false,
diff --git a/src/tribler/ui/src/lib/utils.ts b/src/tribler/ui/src/lib/utils.ts
index f81ad0afc3..24bf59ebfe 100644
--- a/src/tribler/ui/src/lib/utils.ts
+++ b/src/tribler/ui/src/lib/utils.ts
@@ -70,7 +70,7 @@ export function categoryIcon(name: category): string {
 }
 
 export function formatTimeAgo(ts: number) {
-    let locale = triblerService.getGuiSettings().lang ?? 'en-US';
+    let locale = triblerService.guiSettings.lang ?? 'en_US';
     const timeAg = new TimeAgo(locale.slice(0, 2));
     return timeAg.format(ts * 1000);
 }
diff --git a/src/tribler/ui/src/models/settings.model.tsx b/src/tribler/ui/src/models/settings.model.tsx
index d1b8b1b3ab..b3434a7321 100644
--- a/src/tribler/ui/src/models/settings.model.tsx
+++ b/src/tribler/ui/src/models/settings.model.tsx
@@ -96,6 +96,7 @@ export interface Settings {
     },
     state_dir: string;
     memory_db: boolean;
+    ui: GuiSettings;
 }
 
 export interface GuiSettings {
diff --git a/src/tribler/ui/src/pages/Settings/Anonymity.tsx b/src/tribler/ui/src/pages/Settings/Anonymity.tsx
index 9ee6c648d3..5b00d7ff2d 100644
--- a/src/tribler/ui/src/pages/Settings/Anonymity.tsx
+++ b/src/tribler/ui/src/pages/Settings/Anonymity.tsx
@@ -10,7 +10,10 @@ export default function Anonimity() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="p-6 w-full">
diff --git a/src/tribler/ui/src/pages/Settings/Bandwidth.tsx b/src/tribler/ui/src/pages/Settings/Bandwidth.tsx
index 0f746ccf5e..17429426e5 100644
--- a/src/tribler/ui/src/pages/Settings/Bandwidth.tsx
+++ b/src/tribler/ui/src/pages/Settings/Bandwidth.tsx
@@ -11,7 +11,10 @@ export default function Bandwith() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="p-6">
diff --git a/src/tribler/ui/src/pages/Settings/Connection.tsx b/src/tribler/ui/src/pages/Settings/Connection.tsx
index e4a392b88c..edcf324b32 100644
--- a/src/tribler/ui/src/pages/Settings/Connection.tsx
+++ b/src/tribler/ui/src/pages/Settings/Connection.tsx
@@ -13,7 +13,10 @@ export default function Connection() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="px-6 w-full">
diff --git a/src/tribler/ui/src/pages/Settings/Debugging.tsx b/src/tribler/ui/src/pages/Settings/Debugging.tsx
index 5c094b111f..4e53fc0b40 100644
--- a/src/tribler/ui/src/pages/Settings/Debugging.tsx
+++ b/src/tribler/ui/src/pages/Settings/Debugging.tsx
@@ -1,5 +1,5 @@
 import { Checkbox } from "@/components/ui/checkbox";
-import { GuiSettings, Settings } from "@/models/settings.model";
+import { Settings } from "@/models/settings.model";
 import { triblerService } from "@/services/tribler.service";
 import { useState } from "react";
 import { useTranslation } from "react-i18next";
@@ -9,21 +9,25 @@ import SaveButton from "./SaveButton";
 export default function Debugging() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
-    const [guiSettings, setGuiSettings] = useState<GuiSettings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
-    if (!guiSettings) setGuiSettings(triblerService.getGuiSettings());
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="p-6">
             <div className="flex items-center space-x-2 p-2">
                 <Checkbox
-                    checked={guiSettings?.dev_mode === true}
+                    checked={settings?.ui?.dev_mode === true}
                     onCheckedChange={(value) => {
-                        if (guiSettings) {
-                            setGuiSettings({
-                                ...guiSettings,
-                                dev_mode: !!value
+                        if (settings) {
+                            setSettings({
+                                ...settings,
+                                ui: {
+                                    ...settings.ui,
+                                    dev_mode: !!value
+                                }
                             })
 
                         }
@@ -58,12 +62,8 @@ export default function Debugging() {
 
             <SaveButton
                 onClick={async () => {
-                    const refresh = guiSettings?.dev_mode !== triblerService.getGuiSettings().dev_mode;
-                    if (guiSettings)
-                        triblerService.setGuiSettings(guiSettings);
                     if (settings)
                         await triblerService.setSettings(settings);
-                    if (refresh)
                         window.location.reload();
                 }}
             />
diff --git a/src/tribler/ui/src/pages/Settings/General.tsx b/src/tribler/ui/src/pages/Settings/General.tsx
index 69797308e9..6758243411 100644
--- a/src/tribler/ui/src/pages/Settings/General.tsx
+++ b/src/tribler/ui/src/pages/Settings/General.tsx
@@ -1,7 +1,7 @@
 import { PathInput } from "@/components/path-input";
 import { Checkbox } from "@/components/ui/checkbox";
 import { Label } from "@/components/ui/label";
-import { GuiSettings, Settings } from "@/models/settings.model";
+import { Settings } from "@/models/settings.model";
 import { triblerService } from "@/services/tribler.service";
 import { useState } from "react";
 import { useTranslation } from "react-i18next";
@@ -12,10 +12,11 @@ import { Input } from "@/components/ui/input";
 export default function General() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
-    const [guiSettings, setGuiSettings] = useState<GuiSettings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
-    if (!guiSettings) setGuiSettings(triblerService.getGuiSettings());
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="px-6 w-full">
@@ -70,12 +71,15 @@ export default function General() {
             </div>
             <div className="flex items-center space-x-2 py-2">
                 <Checkbox
-                    checked={guiSettings?.ask_download_settings}
+                    checked={settings?.ui?.ask_download_settings}
                     onCheckedChange={(value) => {
                         if (settings) {
-                            setGuiSettings({
+                            setSettings({
                                 ...settings,
-                                ask_download_settings: !!value
+                                ui: {
+                                    ...settings?.ui,
+                                    ask_download_settings: !!value
+                                }
                             });
                         }
                     }}
@@ -141,12 +145,15 @@ export default function General() {
             <div className="pt-5 py-2 font-semibold">{t('FamilyFilter')}</div>
             <div className="flex items-center space-x-2 py-2">
                 <Checkbox
-                    checked={guiSettings?.family_filter}
+                    checked={settings?.ui?.family_filter}
                     onCheckedChange={(value) => {
                         if (settings) {
-                            setGuiSettings({
+                            setSettings({
                                 ...settings,
-                                family_filter: !!value
+                                ui: {
+                                    ...settings?.ui,
+                                    family_filter: !!value
+                                }
                             });
                         }
                     }}
@@ -163,12 +170,15 @@ export default function General() {
             <div className="pt-5 py-2 font-semibold">{t('Tags')}</div>
             <div className="flex items-center space-x-2 py-2">
                 <Checkbox
-                    checked={guiSettings?.disable_tags}
+                    checked={settings?.ui?.disable_tags}
                     onCheckedChange={(value) => {
                         if (settings) {
-                            setGuiSettings({
+                            setSettings({
                                 ...settings,
-                                disable_tags: !!value
+                                ui: {
+                                    ...settings?.ui,
+                                    disable_tags: !!value
+                                }
                             });
                         }
                     }}
@@ -183,8 +193,6 @@ export default function General() {
 
             <SaveButton
                 onClick={async () => {
-                    if (guiSettings)
-                        triblerService.setGuiSettings(guiSettings);
                     if (settings)
                         await triblerService.setSettings(settings);
                 }}
diff --git a/src/tribler/ui/src/pages/Settings/Seeding.tsx b/src/tribler/ui/src/pages/Settings/Seeding.tsx
index c9697994bb..156104abc2 100644
--- a/src/tribler/ui/src/pages/Settings/Seeding.tsx
+++ b/src/tribler/ui/src/pages/Settings/Seeding.tsx
@@ -12,7 +12,10 @@ export default function Seeding() {
     const { t } = useTranslation();
     const [settings, setSettings] = useState<Settings>();
 
-    if (!settings) (async () => { setSettings(await triblerService.getSettings()) })();
+    if (!settings) {
+        (async () => { setSettings(await triblerService.getSettings()) })();
+        return;
+    }
 
     return (
         <div className="p-6 w-full">
diff --git a/src/tribler/ui/src/services/tribler.service.ts b/src/tribler/ui/src/services/tribler.service.ts
index 1c8feb0ebd..aed9a2f89e 100644
--- a/src/tribler/ui/src/services/tribler.service.ts
+++ b/src/tribler/ui/src/services/tribler.service.ts
@@ -11,6 +11,8 @@ export class TriblerService {
     private http: AxiosInstance;
     private baseURL = "/api";
     private events: EventSource;
+    // Store a cached version of the GuiSettings to prevent from having to call the server every time we need them.
+    public guiSettings: GuiSettings = {};
 
     constructor() {
         this.http = axios.create({
@@ -18,6 +20,8 @@ export class TriblerService {
             withCredentials: true,
         });
         this.events = new EventSource(this.baseURL + '/events', { withCredentials: true })
+        // Gets the GuiSettings
+        this.getSettings();
     }
 
     isOnline() {
@@ -26,11 +30,11 @@ export class TriblerService {
 
     // Events
 
-    addEventListener(topic:string, listener: (event: MessageEvent) => void): void {
+    addEventListener(topic: string, listener: (event: MessageEvent) => void): void {
         this.events.addEventListener(topic, listener);
     }
 
-    removeEventListener(topic:string, listener: (event: MessageEvent) => void): void {
+    removeEventListener(topic: string, listener: (event: MessageEvent) => void): void {
         this.events.removeEventListener(topic, listener);
     }
 
@@ -127,7 +131,7 @@ export class TriblerService {
         return (await this.http.get(`/metadata/torrents/popular?metadata_type=300&metadata_type=220&include_total=1&first=1&last=50&hide_xxx=${+hide_xxx}`)).data.results;
     }
 
-    async getTorrentHealth(infohash: string): Promise<{infohash: string, num_seeders: number, num_leechers: number, last_tracker_check: number}> {
+    async getTorrentHealth(infohash: string): Promise<{ infohash: string, num_seeders: number, num_leechers: number, last_tracker_check: number }> {
         return (await this.http.get(`/metadata/torrents/${infohash}/health`)).data;
     }
 
@@ -146,22 +150,14 @@ export class TriblerService {
     // Settings
 
     async getSettings(): Promise<Settings> {
-        return (await this.http.get('/settings')).data.settings;
-    }
-
-    async setSettings(settings: Settings): Promise<boolean> {
-        return (await this.http.post('/settings', settings)).data.modified;
-    }
-
-    getGuiSettings(): GuiSettings {
-        const settings_json = localStorage.getItem("gui_settings") ?? '{"ask_download_settings": true}';
-        const settings: GuiSettings = JSON.parse(settings_json);
+        const settings = (await this.http.get('/settings')).data.settings;
+        this.guiSettings = {...settings?.ui, ...this.guiSettings};
         return settings
     }
 
-    setGuiSettings(settings: GuiSettings) {
-        const settings_json = JSON.stringify(settings);
-        localStorage.setItem("gui_settings", settings_json);
+    async setSettings(settings: Partial<Settings>): Promise<boolean> {
+        this.guiSettings = {...settings?.ui, ...this.guiSettings};
+        return (await this.http.post('/settings', settings)).data.modified;
     }
 
     async getLibtorrentSession(hops: number) {