diff --git a/packages/npm-packages/ruby-wasm-wasi/example/README.md b/packages/npm-packages/ruby-wasm-wasi/example/README.md
index ece5617c2..299491fdb 100644
--- a/packages/npm-packages/ruby-wasm-wasi/example/README.md
+++ b/packages/npm-packages/ruby-wasm-wasi/example/README.md
@@ -17,4 +17,5 @@ $ # Open http://localhost:8000/script-src
 ```console
 $ npm install
 $ node index.node.js
+$ node preopens.node.js
 ```
diff --git a/packages/npm-packages/ruby-wasm-wasi/example/preopens.node.js b/packages/npm-packages/ruby-wasm-wasi/example/preopens.node.js
new file mode 100644
index 000000000..1a16f6b77
--- /dev/null
+++ b/packages/npm-packages/ruby-wasm-wasi/example/preopens.node.js
@@ -0,0 +1,17 @@
+import fs from "fs/promises";
+import { DefaultRubyVM } from "@ruby/wasm-wasi/dist/node";
+
+// $ node preopens.node.js
+
+const binary = await fs.readFile(
+  "./node_modules/@ruby/head-wasm-wasi/dist/ruby.wasm",
+);
+const module = await WebAssembly.compile(binary);
+const { vm } = await DefaultRubyVM(module, {
+  preopens: {
+    "/app": "./require_relative",
+  },
+});
+
+// /app/main.rb uses require_relative to load /app/greeting.rb.
+vm.eval('require "/app/main"');
diff --git a/packages/npm-packages/ruby-wasm-wasi/src/node.ts b/packages/npm-packages/ruby-wasm-wasi/src/node.ts
index 2348510b3..f901a1840 100644
--- a/packages/npm-packages/ruby-wasm-wasi/src/node.ts
+++ b/packages/npm-packages/ruby-wasm-wasi/src/node.ts
@@ -3,9 +3,17 @@ import { RubyVM } from "./vm.js";
 
 export const DefaultRubyVM = async (
   rubyModule: WebAssembly.Module,
-  options: { env?: Record<string, string> | undefined } = {},
+  options: {
+    env?: Record<string, string> | undefined;
+    preopens?: Record<string, string>;
+  } = {},
 ) => {
-  const wasi = new WASI({ env: options.env, version: "preview1", returnOnExit: true });
+  const wasi = new WASI({
+    env: options.env,
+    preopens: options.preopens,
+    version: "preview1",
+    returnOnExit: true,
+  });
   const { vm, instance } = await RubyVM.instantiateModule({ module: rubyModule, wasip1: wasi });
 
   return {
diff --git a/packages/npm-packages/ruby-wasm-wasi/test/package.test.js b/packages/npm-packages/ruby-wasm-wasi/test/package.test.js
index d3924092d..a0352ca67 100644
--- a/packages/npm-packages/ruby-wasm-wasi/test/package.test.js
+++ b/packages/npm-packages/ruby-wasm-wasi/test/package.test.js
@@ -1,5 +1,6 @@
 import * as path from "path";
 import * as fs from "fs/promises";
+import * as os from "os";
 import { WASI } from "wasi";
 import { RubyVM } from "../src/index";
 import { DefaultRubyVM } from "../src/node";
@@ -59,6 +60,52 @@ describe("Packaging validation", () => {
     vm.eval(`require "stringio"`);
   });
 
+  test("DefaultRubyVM WASI preopens with require_relative", async () => {
+    const mod = await loadWasmModule(`ruby+stdlib.wasm`);
+    const tempDir = await fs.mkdtemp(path.join(os.tmpdir(), "ruby-wasm-preopen-"));
+    const nestedDir = path.join(tempDir, "nested");
+    const entryFile = path.join(tempDir, "entry.rb");
+    const helperFile = path.join(nestedDir, "helper.rb");
+
+    try {
+      await fs.mkdir(nestedDir);
+      await fs.writeFile(entryFile, [
+        "PREOPEN_ENTRY_FILE = __FILE__",
+        "require_relative './nested/helper'",
+      ].join("\n"));
+      await fs.writeFile(helperFile, "PREOPEN_HELPER_FILE = __FILE__\n");
+
+      const { vm } = await DefaultRubyVM(mod, {
+        preopens: { "/app": tempDir },
+      });
+      expect(vm.eval(`require "/app/entry"`).toString()).toBe("true");
+      expect(vm.eval(`require "/app/entry"`).toString()).toBe("false");
+
+      expect(vm.eval("PREOPEN_ENTRY_FILE").toString()).toBe("/app/entry.rb");
+      expect(vm.eval("PREOPEN_HELPER_FILE").toString()).toBe(
+        "/app/nested/helper.rb",
+      );
+      expect(
+        vm.eval('$LOADED_FEATURES.include?("/app/entry.rb")').toString(),
+      ).toBe("true");
+      expect(
+        vm
+          .eval('$LOADED_FEATURES.include?("/app/nested/helper.rb")')
+          .toString(),
+      ).toBe("true");
+      expect(
+        vm
+          .eval(`$LOADED_FEATURES.include?(${JSON.stringify(entryFile)})`)
+          .toString(),
+      ).toBe("false");
+      expect(vm.eval(`File.file?(${JSON.stringify(entryFile)})`).toString()).toBe(
+        "false",
+      );
+    } finally {
+      await fs.rm(tempDir, { recursive: true, force: true });
+    }
+  });
+
   test.each([
     { file: "ruby+stdlib.wasm", stdlib: true },
     { file: "ruby.debug+stdlib.wasm", stdlib: true },