diff --git a/.github/workflows/translations-download.yaml b/.github/workflows/translations-download.yaml
index d03040e4..7359f781 100644
--- a/.github/workflows/translations-download.yaml
+++ b/.github/workflows/translations-download.yaml
@@ -24,7 +24,7 @@ jobs:
         run: "yarn install --frozen-lockfile"
 
       - name: Prune i18n
-        run: "rm -R public/locales"
+        run: "rm -R locales"
 
       - name: Download translation files
         uses: localazy/download@0a79880fb66150601e3b43606fab69c88123c087 # v1.1.0
@@ -32,7 +32,7 @@ jobs:
           groups: "-p includeSourceLang:true"
 
       - name: Fix the owner of the downloaded files
-        run: "sudo chown runner:docker -R public/locales"
+        run: "sudo chown runner:docker -R locales"
 
       - name: Prettier
         run: yarn prettier:format
diff --git a/README.md b/README.md
index 43a2dce0..a0af77fc 100644
--- a/README.md
+++ b/README.md
@@ -213,7 +213,7 @@ To add a new translation key you can do these steps:
 
 1. Add the new key entry to the code where the new key is used: `t("some_new_key")`
 1. Run `yarn i18n` to extract the new key and update the translation files. This
-   will add a skeleton entry to the `public/locales/en-GB/app.json` file:
+   will add a skeleton entry to the `locales/en-GB/app.json` file:
    ```jsonc
    {
        ...
@@ -221,7 +221,7 @@ To add a new translation key you can do these steps:
        ...
    }
    ```
-1. Update the skeleton entry in the `public/locales/en-GB/app.json` file with
+1. Update the skeleton entry in the `locales/en-GB/app.json` file with
    the English translation:
 
 ```jsonc
diff --git a/i18next-parser.config.ts b/i18next-parser.config.ts
index f603c37e..7d71d727 100644
--- a/i18next-parser.config.ts
+++ b/i18next-parser.config.ts
@@ -22,7 +22,7 @@ export default {
     ],
   },
   locales: ["en-GB"],
-  output: "public/locales/$LOCALE/$NAMESPACE.json",
+  output: "locales/$LOCALE/$NAMESPACE.json",
   input: ["src/**/*.{ts,tsx}"],
   sort: true,
 };
diff --git a/localazy.json b/localazy.json
index 41cb7656..2b9f713c 100644
--- a/localazy.json
+++ b/localazy.json
@@ -7,13 +7,13 @@
     "features": ["plural_postfix_us", "filter_untranslated"],
     "files": [
       {
-        "pattern": "public/locales/en-GB/*.json",
+        "pattern": "locales/en-GB/*.json",
         "lang": "inherited"
       },
       {
         "group": "existing",
-        "pattern": "public/locales/*/*.json",
-        "excludes": ["public/locales/en-GB/*.json"],
+        "pattern": "locales/*/*.json",
+        "excludes": ["locales/en-GB/*.json"],
         "lang": "${autodetectLang}"
       }
     ]
@@ -22,7 +22,7 @@
   "download": {
     "files": [
       {
-        "output": "public/locales/${langLsrDash}/${file}"
+        "output": "locales/${langLsrDash}/${file}"
       }
     ],
     "includeSourceLang": "${includeSourceLang|false}",
diff --git a/public/locales/bg/app.json b/locales/bg/app.json
similarity index 100%
rename from public/locales/bg/app.json
rename to locales/bg/app.json
diff --git a/public/locales/cs/app.json b/locales/cs/app.json
similarity index 100%
rename from public/locales/cs/app.json
rename to locales/cs/app.json
diff --git a/public/locales/de/app.json b/locales/de/app.json
similarity index 100%
rename from public/locales/de/app.json
rename to locales/de/app.json
diff --git a/public/locales/el/app.json b/locales/el/app.json
similarity index 100%
rename from public/locales/el/app.json
rename to locales/el/app.json
diff --git a/public/locales/en-GB/app.json b/locales/en-GB/app.json
similarity index 100%
rename from public/locales/en-GB/app.json
rename to locales/en-GB/app.json
diff --git a/public/locales/es/app.json b/locales/es/app.json
similarity index 100%
rename from public/locales/es/app.json
rename to locales/es/app.json
diff --git a/public/locales/et/app.json b/locales/et/app.json
similarity index 100%
rename from public/locales/et/app.json
rename to locales/et/app.json
diff --git a/public/locales/fa/app.json b/locales/fa/app.json
similarity index 100%
rename from public/locales/fa/app.json
rename to locales/fa/app.json
diff --git a/public/locales/fr/app.json b/locales/fr/app.json
similarity index 100%
rename from public/locales/fr/app.json
rename to locales/fr/app.json
diff --git a/public/locales/id/app.json b/locales/id/app.json
similarity index 100%
rename from public/locales/id/app.json
rename to locales/id/app.json
diff --git a/public/locales/it/app.json b/locales/it/app.json
similarity index 100%
rename from public/locales/it/app.json
rename to locales/it/app.json
diff --git a/public/locales/ja/app.json b/locales/ja/app.json
similarity index 100%
rename from public/locales/ja/app.json
rename to locales/ja/app.json
diff --git a/public/locales/lv/app.json b/locales/lv/app.json
similarity index 100%
rename from public/locales/lv/app.json
rename to locales/lv/app.json
diff --git a/public/locales/pl/app.json b/locales/pl/app.json
similarity index 100%
rename from public/locales/pl/app.json
rename to locales/pl/app.json
diff --git a/public/locales/ru/app.json b/locales/ru/app.json
similarity index 100%
rename from public/locales/ru/app.json
rename to locales/ru/app.json
diff --git a/public/locales/sk/app.json b/locales/sk/app.json
similarity index 100%
rename from public/locales/sk/app.json
rename to locales/sk/app.json
diff --git a/public/locales/sv/app.json b/locales/sv/app.json
similarity index 100%
rename from public/locales/sv/app.json
rename to locales/sv/app.json
diff --git a/public/locales/tr/app.json b/locales/tr/app.json
similarity index 100%
rename from public/locales/tr/app.json
rename to locales/tr/app.json
diff --git a/public/locales/uk/app.json b/locales/uk/app.json
similarity index 100%
rename from public/locales/uk/app.json
rename to locales/uk/app.json
diff --git a/public/locales/vi/app.json b/locales/vi/app.json
similarity index 100%
rename from public/locales/vi/app.json
rename to locales/vi/app.json
diff --git a/public/locales/zh-Hans/app.json b/locales/zh-Hans/app.json
similarity index 100%
rename from public/locales/zh-Hans/app.json
rename to locales/zh-Hans/app.json
diff --git a/public/locales/zh-Hant/app.json b/locales/zh-Hant/app.json
similarity index 100%
rename from public/locales/zh-Hant/app.json
rename to locales/zh-Hant/app.json
diff --git a/package.json b/package.json
index b1015050..0515578e 100644
--- a/package.json
+++ b/package.json
@@ -84,7 +84,6 @@
     "history": "^4.0.0",
     "i18next": "^23.0.0",
     "i18next-browser-languagedetector": "^8.0.0",
-    "i18next-http-backend": "^2.0.0",
     "i18next-parser": "^9.0.0",
     "jsdom": "^25.0.0",
     "knip": "^5.27.2",
diff --git a/src/@types/i18next.d.ts b/src/@types/i18next.d.ts
index ad35f456..4a8830da 100644
--- a/src/@types/i18next.d.ts
+++ b/src/@types/i18next.d.ts
@@ -7,7 +7,7 @@ Please see LICENSE in the repository root for full details.
 
 import "i18next";
 // import all namespaces (for the default language, only)
-import app from "../../public/locales/en-GB/app.json";
+import app from "../../locales/en-GB/app.json";
 
 declare module "i18next" {
   interface CustomTypeOptions {
diff --git a/src/initializer.tsx b/src/initializer.tsx
index 0ac8a88a..47634078 100644
--- a/src/initializer.tsx
+++ b/src/initializer.tsx
@@ -5,10 +5,13 @@ SPDX-License-Identifier: AGPL-3.0-only
 Please see LICENSE in the repository root for full details.
 */
 
-import i18n from "i18next";
+import i18n, {
+  type BackendModule,
+  type ReadCallback,
+  type ResourceKey,
+} from "i18next";
 import { initReactI18next } from "react-i18next";
 import LanguageDetector from "i18next-browser-languagedetector";
-import Backend from "i18next-http-backend";
 import * as Sentry from "@sentry/react";
 import { logger } from "matrix-js-sdk/src/logger";
 import { shouldPolyfill as shouldPolyfillSegmenter } from "@formatjs/intl-segmenter/should-polyfill";
@@ -19,6 +22,68 @@ import { Config } from "./config/Config";
 import { ElementCallOpenTelemetry } from "./otel/otel";
 import { platform } from "./Platform";
 
+// This generates a map of locale names to their URL (based on import.meta.url), which looks like this:
+// {
+//   "../locales/en-GB/app.json": "/whatever/assets/root/locales/en-aabbcc.json",
+//   ...
+// }
+const locales = import.meta.glob<string>("../locales/*/*.json", {
+  query: "?url",
+  import: "default",
+  eager: true,
+});
+
+const getLocaleUrl = (
+  language: string,
+  namespace: string,
+): string | undefined => locales[`../locales/${language}/${namespace}.json`];
+
+const supportedLngs = [
+  ...new Set(
+    Object.keys(locales).map((url) => {
+      // The URLs are of the form ../locales/en-GB/app.json
+      // This extracts the language code from the URL
+      const lang = url.match(/\/([^/]+)\/[^/]+\.json$/)?.[1];
+      if (!lang) {
+        throw new Error(`Could not parse locale URL ${url}`);
+      }
+      return lang;
+    }),
+  ),
+];
+
+// A backend that fetches the locale files from the URLs generated by the glob above
+const Backend = {
+  type: "backend",
+  init(): void {},
+  read(language: string, namespace: string, callback: ReadCallback): void {
+    (async (): Promise<ResourceKey> => {
+      const url = getLocaleUrl(language, namespace);
+      if (!url) {
+        throw new Error(
+          `Namespace ${namespace} for locale ${language} not found`,
+        );
+      }
+
+      const response = await fetch(url, {
+        credentials: "omit",
+        headers: {
+          Accept: "application/json",
+        },
+      });
+
+      if (!response.ok) {
+        throw Error(`Failed to fetch ${url}`);
+      }
+
+      return await response.json();
+    })().then(
+      (data) => callback(null, data),
+      (error) => callback(error, null),
+    );
+  },
+} satisfies BackendModule;
+
 enum LoadState {
   None,
   Loading,
@@ -74,6 +139,7 @@ export class Initializer {
         nsSeparator: false,
         pluralSeparator: "_",
         contextSeparator: "|",
+        supportedLngs,
         interpolation: {
           escapeValue: false, // React has built-in XSS protections
         },
diff --git a/src/vitest.setup.ts b/src/vitest.setup.ts
index 776a13b0..421ec663 100644
--- a/src/vitest.setup.ts
+++ b/src/vitest.setup.ts
@@ -16,7 +16,7 @@ import { cleanup } from "@testing-library/react";
 import "vitest-axe/extend-expect";
 import { logger } from "matrix-js-sdk/src/logger";
 
-import EN_GB from "../public/locales/en-GB/app.json";
+import EN_GB from "../locales/en-GB/app.json";
 import { Config } from "./config/Config";
 
 // Bare-minimum i18n config
diff --git a/vite.config.js b/vite.config.js
index b92f717b..6c714bcb 100644
--- a/vite.config.js
+++ b/vite.config.js
@@ -60,6 +60,25 @@ export default defineConfig(({ mode }) => {
     },
     build: {
       sourcemap: true,
+      rollupOptions: {
+        output: {
+          assetFileNames: ({ originalFileNames }) => {
+            if (originalFileNames) {
+              for (const name of originalFileNames) {
+                // Custom asset name for locales to include the locale code in the filename
+                const match = name.match(/locales\/([^/]+)\/(.+)\.json$/);
+                if (match) {
+                  const [, locale, filename] = match;
+                  return `assets/${locale}-${filename}-[hash].json`;
+                }
+              }
+            }
+
+            // Default naming fallback
+            return "assets/[name]-[hash][extname]";
+          },
+        },
+      },
     },
     plugins,
     resolve: {
diff --git a/yarn.lock b/yarn.lock
index 5057090b..42c6e6b0 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -4138,13 +4138,6 @@ cosmiconfig@^8.1.3:
     parse-json "^5.2.0"
     path-type "^4.0.0"
 
-cross-fetch@4.0.0:
-  version "4.0.0"
-  resolved "https://registry.yarnpkg.com/cross-fetch/-/cross-fetch-4.0.0.tgz#f037aef1580bb3a1a35164ea2a848ba81b445983"
-  integrity sha512-e4a5N8lVvuLgAWgnCrLr2PP0YyDOTHa9H/Rj54dirp61qXnNq46m82bRhNqIA5VccJtWBvPTFRV3TtvHUKPB1g==
-  dependencies:
-    node-fetch "^2.6.12"
-
 cross-spawn@^7.0.0, cross-spawn@^7.0.2:
   version "7.0.3"
   resolved "https://registry.yarnpkg.com/cross-spawn/-/cross-spawn-7.0.3.tgz#f73a85b9d5d41d045551c177e2882d4ac85728a6"
@@ -5469,13 +5462,6 @@ i18next-browser-languagedetector@^8.0.0:
   dependencies:
     "@babel/runtime" "^7.23.2"
 
-i18next-http-backend@^2.0.0:
-  version "2.6.2"
-  resolved "https://registry.yarnpkg.com/i18next-http-backend/-/i18next-http-backend-2.6.2.tgz#b25516446ae6f251ce8231e70e6ffbca833d46a5"
-  integrity sha512-Hp/kd8/VuoxIHmxsknJXjkTYYHzivAyAF15pzliKzk2TiXC25rZCEerb1pUFoxz4IVrG3fCvQSY51/Lu4ECV4A==
-  dependencies:
-    cross-fetch "4.0.0"
-
 i18next-parser@^9.0.0:
   version "9.0.2"
   resolved "https://registry.yarnpkg.com/i18next-parser/-/i18next-parser-9.0.2.tgz#f9d627422d33c352967556c8724975d58f1f5a95"
@@ -6331,7 +6317,7 @@ node-addon-api@^7.0.0:
   resolved "https://registry.yarnpkg.com/node-addon-api/-/node-addon-api-7.1.1.tgz#1aba6693b0f255258a049d621329329322aad558"
   integrity sha512-5m3bsyrjFWE1xf7nz7YXdN4udnVtXK6/Yfgn5qnahL6bCkf2yKt4k3nuTKAtT4r3IG8JNR2ncsIMdZuAzJjHQQ==
 
-node-fetch@^2.6.12, node-fetch@^2.6.7:
+node-fetch@^2.6.7:
   version "2.7.0"
   resolved "https://registry.yarnpkg.com/node-fetch/-/node-fetch-2.7.0.tgz#d0f0fa6e3e2dc1d27efcd8ad99d550bda94d187d"
   integrity sha512-c4FRfUm/dbcWZ7U+1Wq0AwCyFL+3nt2bEw05wfxSz+DWpWsitgmSgYmy2dQdWyKC1694ELPqMs/YzUSNozLt8A==