diff --git a/integration/helpers/node-template/package.json b/integration/helpers/node-template/package.json
index 1d26acc8cfb..2f477337507 100644
--- a/integration/helpers/node-template/package.json
+++ b/integration/helpers/node-template/package.json
@@ -23,8 +23,9 @@
   },
   "devDependencies": {
     "@remix-run/dev": "workspace:*",
-    "@remix-run/route-config": "workspace:*",
     "@remix-run/fs-routes": "workspace:*",
+    "@remix-run/route-config": "workspace:*",
+    "@remix-run/routes-option-adapter": "workspace:*",
     "@vanilla-extract/css": "^1.10.0",
     "@vanilla-extract/vite-plugin": "^3.9.2",
     "@types/react": "^18.2.20",
diff --git a/integration/vite-fs-routes-test.ts b/integration/vite-fs-routes-test.ts
index e3709d99967..5e9f9d44545 100644
--- a/integration/vite-fs-routes-test.ts
+++ b/integration/vite-fs-routes-test.ts
@@ -29,11 +29,22 @@ test.describe("fs-routes", () => {
         "app/routes.ts": js`
           import { type RouteConfig } from "@remix-run/route-config";  
           import { flatRoutes } from "@remix-run/fs-routes";
-
-          export const routes: RouteConfig = flatRoutes({
-            rootDirectory: "fs-routes",
-            ignoredRouteFiles: ["**/ignored-route.*"],
-          });
+          import { routesOptionAdapter } from "@remix-run/routes-option-adapter";
+
+          export const routes: RouteConfig = [
+            ...await flatRoutes({
+              rootDirectory: "fs-routes",
+              ignoredRouteFiles: ["**/ignored-route.*"],
+            }),
+
+            // Ensure back compat layer works
+            ...await routesOptionAdapter(async (defineRoutes) => {
+              // Ensure async routes work
+              return defineRoutes((route) => {
+                route("/routes/option/adapter/route", "routes-option-adapter-route.tsx")
+              });
+            })
+          ];
         `,
         "app/root.tsx": js`
           import { Links, Meta, Outlet, Scripts } from "@remix-run/react";
@@ -81,6 +92,12 @@ test.describe("fs-routes", () => {
           }
         `,
 
+        "app/routes-option-adapter-route.tsx": js`
+          export default function () {
+            return <h2>Routes Option Adapter Route</h2>;
+          }
+        `,
+
         "app/fs-routes/.dotfile": `
           DOTFILE SHOULD BE IGNORED
         `,
@@ -176,6 +193,17 @@ test.describe("fs-routes", () => {
 </div>`);
     });
 
+    test("renders matching routes (routes option adapter)", async ({
+      page,
+    }) => {
+      let app = new PlaywrightFixture(appFixture, page);
+      await app.goto("/routes/option/adapter/route");
+      expect(await app.getHtml("#content")).toBe(`<div id="content">
+  <h1>Root</h1>
+  <h2>Routes Option Adapter Route</h2>
+</div>`);
+    });
+
     test("renders matching routes (route with escaped leading dot)", async ({
       page,
     }) => {
diff --git a/packages/remix-fs-routes/__tests__/routeManifestToRouteConfig-test.ts b/packages/remix-dev/__tests__/routeManifestToRouteConfig-test.ts
similarity index 80%
rename from packages/remix-fs-routes/__tests__/routeManifestToRouteConfig-test.ts
rename to packages/remix-dev/__tests__/routeManifestToRouteConfig-test.ts
index d4e9be71597..a236c022ada 100644
--- a/packages/remix-fs-routes/__tests__/routeManifestToRouteConfig-test.ts
+++ b/packages/remix-dev/__tests__/routeManifestToRouteConfig-test.ts
@@ -1,6 +1,4 @@
-import { route } from "@remix-run/route-config";
-
-import { routeManifestToRouteConfig } from "../manifest";
+import { type RouteConfig, routeManifestToRouteConfig } from "../config/routes";
 
 const clean = (obj: any) => cleanUndefined(cleanIds(obj));
 
@@ -43,14 +41,27 @@ describe("routeManifestToRouteConfig", () => {
         caseSensitive: true,
       },
     });
-    let routeConfig = [
-      route("/", "routes/home.js"),
-      route("inbox", "routes/inbox.js", [
-        route("/", "routes/inbox/index.js", { index: true }),
-        route(":messageId", "routes/inbox/$messageId.js", {
-          caseSensitive: true,
-        }),
-      ]),
+    let routeConfig: RouteConfig = [
+      {
+        path: "/",
+        file: "routes/home.js",
+      },
+      {
+        path: "inbox",
+        file: "routes/inbox.js",
+        children: [
+          {
+            path: "/",
+            file: "routes/inbox/index.js",
+            index: true,
+          },
+          {
+            path: ":messageId",
+            file: "routes/inbox/$messageId.js",
+            caseSensitive: true,
+          },
+        ],
+      },
     ];
 
     expect(clean(routeManifestConfig)).toEqual(clean(routeConfig));
diff --git a/packages/remix-dev/config/routes.ts b/packages/remix-dev/config/routes.ts
index fd4dd22cbbf..3e2b919517c 100644
--- a/packages/remix-dev/config/routes.ts
+++ b/packages/remix-dev/config/routes.ts
@@ -57,6 +57,45 @@ export interface RouteManifest {
   [routeId: string]: RouteManifestEntry;
 }
 
+export function routeManifestToRouteConfig(
+  routeManifest: RouteManifest,
+  rootId = "root"
+): RouteConfigEntry[] {
+  let routeConfigById: {
+    [id: string]: Omit<RouteConfigEntry, "id"> &
+      Required<Pick<RouteConfigEntry, "id">>;
+  } = {};
+
+  for (let id in routeManifest) {
+    let route = routeManifest[id];
+    routeConfigById[id] = {
+      id: route.id,
+      file: route.file,
+      path: route.path,
+      index: route.index,
+      caseSensitive: route.caseSensitive,
+    };
+  }
+
+  let routeConfig: RouteConfigEntry[] = [];
+
+  for (let id in routeConfigById) {
+    let route = routeConfigById[id];
+    let parentId = routeManifest[route.id].parentId;
+    if (parentId === rootId) {
+      routeConfig.push(route);
+    } else {
+      let parentRoute = parentId && routeConfigById[parentId];
+      if (parentRoute) {
+        parentRoute.children = parentRoute.children || [];
+        parentRoute.children.push(route);
+      }
+    }
+  }
+
+  return routeConfig;
+}
+
 /**
  * Configuration for an individual route, for use within `routes.ts`. As a
  * convenience, route config entries can be created with the {@link route},
diff --git a/packages/remix-dev/index.ts b/packages/remix-dev/index.ts
index 38581e081f7..baabf348966 100644
--- a/packages/remix-dev/index.ts
+++ b/packages/remix-dev/index.ts
@@ -6,10 +6,17 @@ export * as cli from "./cli/index";
 
 export type { Manifest as AssetsManifest } from "./manifest";
 export type {
+  DefineRoutesFunction as UNSAFE_DefineRoutesFunction,
+  RouteManifest as UNSAFE_RouteManifest,
+  RouteManifestEntry as UNSAFE_RouteManifestEntry,
   RouteConfig as UNSAFE_RouteConfig,
   RouteConfigEntry as UNSAFE_RouteConfigEntry,
 } from "./config/routes";
-export { getRouteConfigAppDirectory as UNSAFE_getRouteConfigAppDirectory } from "./config/routes";
+export {
+  defineRoutes as UNSAFE_defineRoutes,
+  routeManifestToRouteConfig as UNSAFE_routeManifestToRouteConfig,
+  getRouteConfigAppDirectory as UNSAFE_getRouteConfigAppDirectory,
+} from "./config/routes";
 export { getDependenciesToBundle } from "./dependencies";
 export type {
   BuildManifest,
diff --git a/packages/remix-fs-routes/flatRoutes.ts b/packages/remix-fs-routes/flatRoutes.ts
index 4195f735a4c..9d48763b9dc 100644
--- a/packages/remix-fs-routes/flatRoutes.ts
+++ b/packages/remix-fs-routes/flatRoutes.ts
@@ -1,8 +1,11 @@
 import fs from "node:fs";
 import path from "node:path";
 import { makeRe } from "minimatch";
+import type {
+  UNSAFE_RouteManifest as RouteManifest,
+  UNSAFE_RouteManifestEntry as RouteManifestEntry,
+} from "@remix-run/dev";
 
-import type { RouteManifest, RouteManifestEntry } from "./manifest";
 import { normalizeSlashes } from "./normalizeSlashes";
 
 export const routeModuleExts = [".js", ".jsx", ".ts", ".tsx", ".md", ".mdx"];
diff --git a/packages/remix-fs-routes/index.ts b/packages/remix-fs-routes/index.ts
index a0ccc39fefd..faf5ea44c63 100644
--- a/packages/remix-fs-routes/index.ts
+++ b/packages/remix-fs-routes/index.ts
@@ -1,11 +1,11 @@
 import fs from "node:fs";
 import path from "node:path";
+import { UNSAFE_routeManifestToRouteConfig as routeManifestToRouteConfig } from "@remix-run/dev";
 import {
   type RouteConfigEntry,
   getAppDirectory,
 } from "@remix-run/route-config";
 
-import { routeManifestToRouteConfig } from "./manifest";
 import { flatRoutes as flatRoutesImpl } from "./flatRoutes";
 import { normalizeSlashes } from "./normalizeSlashes";
 
diff --git a/packages/remix-fs-routes/manifest.ts b/packages/remix-fs-routes/manifest.ts
deleted file mode 100644
index 3b9ea7ae1d8..00000000000
--- a/packages/remix-fs-routes/manifest.ts
+++ /dev/null
@@ -1,53 +0,0 @@
-import type { RouteConfigEntry } from "@remix-run/route-config";
-
-export interface RouteManifestEntry {
-  path?: string;
-  index?: boolean;
-  caseSensitive?: boolean;
-  id: string;
-  parentId?: string;
-  file: string;
-}
-
-export interface RouteManifest {
-  [routeId: string]: RouteManifestEntry;
-}
-
-export function routeManifestToRouteConfig(
-  routeManifest: RouteManifest,
-  rootId = "root"
-): RouteConfigEntry[] {
-  let routeConfigById: {
-    [id: string]: Omit<RouteConfigEntry, "id"> &
-      Required<Pick<RouteConfigEntry, "id">>;
-  } = {};
-
-  for (let id in routeManifest) {
-    let route = routeManifest[id];
-    routeConfigById[id] = {
-      id: route.id,
-      file: route.file,
-      path: route.path,
-      index: route.index,
-      caseSensitive: route.caseSensitive,
-    };
-  }
-
-  let routeConfig: RouteConfigEntry[] = [];
-
-  for (let id in routeConfigById) {
-    let route = routeConfigById[id];
-    let parentId = routeManifest[route.id].parentId;
-    if (parentId === rootId) {
-      routeConfig.push(route);
-    } else {
-      let parentRoute = parentId && routeConfigById[parentId];
-      if (parentRoute) {
-        parentRoute.children = parentRoute.children || [];
-        parentRoute.children.push(route);
-      }
-    }
-  }
-
-  return routeConfig;
-}
diff --git a/packages/remix-fs-routes/package.json b/packages/remix-fs-routes/package.json
index 5f803ade36b..75b82093267 100644
--- a/packages/remix-fs-routes/package.json
+++ b/packages/remix-fs-routes/package.json
@@ -1,7 +1,7 @@
 {
   "name": "@remix-run/fs-routes",
   "version": "2.13.1",
-  "description": "Config-based file system routing conventions for Remix",
+  "description": "Config-based file system routing conventions, for use within routes.ts",
   "bugs": {
     "url": "https://github.com/remix-run/remix/issues"
   },
@@ -27,10 +27,12 @@
     "minimatch": "^9.0.0"
   },
   "devDependencies": {
+    "@remix-run/dev": "workspace:*",
     "@remix-run/route-config": "workspace:*",
     "typescript": "^5.1.6"
   },
   "peerDependencies": {
+    "@remix-run/dev": "workspace:*",
     "@remix-run/route-config": "workspace:*",
     "typescript": "^5.1.0"
   },
diff --git a/packages/remix-route-config/package.json b/packages/remix-route-config/package.json
index 574c8c042c0..701968b67e9 100644
--- a/packages/remix-route-config/package.json
+++ b/packages/remix-route-config/package.json
@@ -1,14 +1,14 @@
 {
   "name": "@remix-run/route-config",
   "version": "2.13.1",
-  "description": "Config-based routing for Remix",
+  "description": "Config-based routing utilities, for use within routes.ts",
   "bugs": {
     "url": "https://github.com/remix-run/remix/issues"
   },
   "repository": {
     "type": "git",
     "url": "https://github.com/remix-run/remix",
-    "directory": "packages/remix-fs-routes"
+    "directory": "packages/remix-route-config"
   },
   "license": "MIT",
   "main": "dist/index.js",
diff --git a/packages/remix-routes-option-adapter/README.md b/packages/remix-routes-option-adapter/README.md
new file mode 100644
index 00000000000..40685a7476f
--- /dev/null
+++ b/packages/remix-routes-option-adapter/README.md
@@ -0,0 +1,13 @@
+# Welcome to Remix!
+
+[Remix](https://remix.run) is a web framework that helps you build better websites with React.
+
+To get started, open a new shell and run:
+
+```sh
+npx create-remix@latest
+```
+
+Then follow the prompts you see in your terminal.
+
+For more information about Remix, [visit remix.run](https://remix.run)!
diff --git a/packages/remix-routes-option-adapter/index.ts b/packages/remix-routes-option-adapter/index.ts
new file mode 100644
index 00000000000..bc16aa18fa8
--- /dev/null
+++ b/packages/remix-routes-option-adapter/index.ts
@@ -0,0 +1,24 @@
+import {
+  type UNSAFE_DefineRoutesFunction as DefineRoutesFunction,
+  UNSAFE_defineRoutes as defineRoutes,
+  UNSAFE_routeManifestToRouteConfig as routeManifestToRouteConfig,
+} from "@remix-run/dev";
+import { type RouteConfigEntry } from "@remix-run/route-config";
+
+export type { DefineRoutesFunction };
+
+/**
+ * Adapter for [Remix's `routes` config
+ * option](https://remix.run/docs/en/v2/file-conventions/vite-config#routes),
+ * for use within `routes.ts`.
+ */
+export async function routesOptionAdapter(
+  routes: (
+    defineRoutes: DefineRoutesFunction
+  ) =>
+    | ReturnType<DefineRoutesFunction>
+    | Promise<ReturnType<DefineRoutesFunction>>
+): Promise<RouteConfigEntry[]> {
+  let routeManifest = await routes(defineRoutes);
+  return routeManifestToRouteConfig(routeManifest);
+}
diff --git a/packages/remix-routes-option-adapter/package.json b/packages/remix-routes-option-adapter/package.json
new file mode 100644
index 00000000000..529b43c5531
--- /dev/null
+++ b/packages/remix-routes-option-adapter/package.json
@@ -0,0 +1,53 @@
+{
+  "name": "@remix-run/routes-option-adapter",
+  "version": "2.13.1",
+  "description": "Adapter for Remix's \"routes\" config option, for use within routes.ts",
+  "bugs": {
+    "url": "https://github.com/remix-run/remix/issues"
+  },
+  "repository": {
+    "type": "git",
+    "url": "https://github.com/remix-run/remix",
+    "directory": "packages/remix-routes-option-adapter"
+  },
+  "license": "MIT",
+  "main": "dist/index.js",
+  "typings": "dist/index.d.ts",
+  "exports": {
+    ".": {
+      "types": "./dist/index.d.ts",
+      "default": "./dist/index.js"
+    },
+    "./package.json": "./package.json"
+  },
+  "scripts": {
+    "tsc": "tsc"
+  },
+  "dependencies": {
+    "minimatch": "^9.0.0"
+  },
+  "devDependencies": {
+    "@remix-run/dev": "workspace:*",
+    "@remix-run/route-config": "workspace:*",
+    "typescript": "^5.1.6"
+  },
+  "peerDependencies": {
+    "@remix-run/dev": "workspace:*",
+    "@remix-run/route-config": "workspace:*",
+    "typescript": "^5.1.0"
+  },
+  "peerDependenciesMeta": {
+    "typescript": {
+      "optional": true
+    }
+  },
+  "engines": {
+    "node": ">=18.0.0"
+  },
+  "files": [
+    "dist/",
+    "CHANGELOG.md",
+    "LICENSE.md",
+    "README.md"
+  ]
+}
diff --git a/packages/remix-routes-option-adapter/rollup.config.js b/packages/remix-routes-option-adapter/rollup.config.js
new file mode 100644
index 00000000000..59e7189afe3
--- /dev/null
+++ b/packages/remix-routes-option-adapter/rollup.config.js
@@ -0,0 +1,45 @@
+const path = require("node:path");
+const babel = require("@rollup/plugin-babel").default;
+const nodeResolve = require("@rollup/plugin-node-resolve").default;
+const copy = require("rollup-plugin-copy");
+
+const {
+  copyToPlaygrounds,
+  createBanner,
+  getOutputDir,
+  isBareModuleId,
+} = require("../../rollup.utils");
+const { name: packageName, version } = require("./package.json");
+
+/** @returns {import("rollup").RollupOptions[]} */
+module.exports = function rollup() {
+  let sourceDir = "packages/remix-routes-option-adapter";
+  let outputDir = getOutputDir(packageName);
+  let outputDist = path.join(outputDir, "dist");
+
+  return [
+    {
+      external: (id) => isBareModuleId(id),
+      input: `${sourceDir}/index.ts`,
+      output: {
+        banner: createBanner(packageName, version),
+        dir: outputDist,
+        format: "cjs",
+        preserveModules: true,
+        exports: "auto",
+      },
+      plugins: [
+        babel({
+          babelHelpers: "bundled",
+          exclude: /node_modules/,
+          extensions: [".ts"],
+        }),
+        nodeResolve({ extensions: [".ts"] }),
+        copy({
+          targets: [{ src: "LICENSE.md", dest: sourceDir }],
+        }),
+        copyToPlaygrounds(),
+      ],
+    },
+  ];
+};
diff --git a/packages/remix-routes-option-adapter/tsconfig.json b/packages/remix-routes-option-adapter/tsconfig.json
new file mode 100644
index 00000000000..897cf7dd585
--- /dev/null
+++ b/packages/remix-routes-option-adapter/tsconfig.json
@@ -0,0 +1,19 @@
+{
+  "include": ["**/*.ts"],
+  "exclude": ["dist", "__tests__", "node_modules"],
+  "compilerOptions": {
+    "lib": ["DOM", "DOM.Iterable", "ES2022"],
+    "target": "ES2022",
+    "module": "ES2022",
+    "skipLibCheck": true,
+
+    "moduleResolution": "Bundler",
+    "allowSyntheticDefaultImports": true,
+    "strict": true,
+    "jsx": "react",
+    "declaration": true,
+    "emitDeclarationOnly": true,
+    "rootDir": ".",
+    "outDir": "../../build/node_modules/@remix-run/routes-option-adapter/dist"
+  }
+}
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index 502368f25bd..3ee9624be80 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -526,6 +526,9 @@ importers:
       '@remix-run/route-config':
         specifier: workspace:*
         version: link:../../../packages/remix-route-config
+      '@remix-run/routes-option-adapter':
+        specifier: workspace:*
+        version: link:../../../packages/remix-routes-option-adapter
       '@types/react':
         specifier: ^18.2.20
         version: 18.2.20
@@ -1201,6 +1204,9 @@ importers:
         specifier: ^9.0.0
         version: 9.0.3
     devDependencies:
+      '@remix-run/dev':
+        specifier: workspace:*
+        version: link:../remix-dev
       '@remix-run/route-config':
         specifier: workspace:*
         version: link:../remix-route-config
@@ -1307,6 +1313,22 @@ importers:
         specifier: 5.1.8
         version: 5.1.8(@types/node@18.17.1)
 
+  packages/remix-routes-option-adapter:
+    dependencies:
+      minimatch:
+        specifier: ^9.0.0
+        version: 9.0.3
+    devDependencies:
+      '@remix-run/dev':
+        specifier: workspace:*
+        version: link:../remix-dev
+      '@remix-run/route-config':
+        specifier: workspace:*
+        version: link:../remix-route-config
+      typescript:
+        specifier: ^5.1.6
+        version: 5.1.6
+
   packages/remix-serve:
     dependencies:
       '@remix-run/express':
diff --git a/pnpm-workspace.yaml b/pnpm-workspace.yaml
index 8671741fd4c..e8c91c3e82c 100644
--- a/pnpm-workspace.yaml
+++ b/pnpm-workspace.yaml
@@ -20,6 +20,7 @@ packages:
   - "packages/remix-node"
   - "packages/remix-react"
   - "packages/remix-route-config"
+  - "packages/remix-routes-option-adapter"
   - "packages/remix-serve"
   - "packages/remix-server-runtime"
   - "packages/remix-testing"
diff --git a/scripts/publish.js b/scripts/publish.js
index 5300a854af8..37fa8f7f37b 100644
--- a/scripts/publish.js
+++ b/scripts/publish.js
@@ -64,6 +64,7 @@ async function run() {
     "css-bundle",
     "testing",
     "route-config",
+    "routes-option-adapter",
   ]) {
     publish(path.join(buildDir, "@remix-run", name), tag);
   }