diff --git a/src/js/node/wasi.ts b/src/js/node/wasi.ts
index a0ae57df5c5c..0a8de0c85b1a 100644
--- a/src/js/node/wasi.ts
+++ b/src/js/node/wasi.ts
@@ -1437,7 +1437,7 @@ var require_wasi = __commonJS({
           path_open: wrap(
             (dirfd, _dirflags, pathPtr, pathLen, oflags, fsRightsBase, fsRightsInheriting, fsFlags, fdPtr) => {
               try {
-                CHECK_FD(dirfd, constants_1.WASI_RIGHT_PATH_OPEN);
+                const stats = CHECK_FD(dirfd, constants_1.WASI_RIGHT_PATH_OPEN);
                 fsRightsBase = BigInt(fsRightsBase);
                 fsRightsInheriting = BigInt(fsRightsInheriting);
                 const read =
@@ -1512,7 +1512,7 @@ var require_wasi = __commonJS({
                 if (p.startsWith("proc/")) {
                   throw new types_1.WASIError(constants_1.WASI_EBADF);
                 }
-                const fullUnresolved = path.resolve(p);
+                const fullUnresolved = path.resolve(stats.path, p);
                 let full;
                 try {
                   full = fs.realpathSync(fullUnresolved);
diff --git a/test/js/bun/wasm/read-file.wasm b/test/js/bun/wasm/read-file.wasm
new file mode 100755
index 000000000000..603b46273337
Binary files /dev/null and b/test/js/bun/wasm/read-file.wasm differ
diff --git a/test/js/bun/wasm/wasi.test.js b/test/js/bun/wasm/wasi.test.js
index 5e6994a50457..3e0f0b5f328a 100644
--- a/test/js/bun/wasm/wasi.test.js
+++ b/test/js/bun/wasm/wasi.test.js
@@ -1,6 +1,6 @@
 import { spawnSync } from "bun";
 import { expect, it } from "bun:test";
-import { bunEnv, bunExe } from "harness";
+import { bunEnv, bunExe, tempDirWithFiles } from "harness";
 
 it("Should support printing 'hello world'", () => {
   const { stdout, stderr, exitCode } = spawnSync({
@@ -20,3 +20,43 @@ it("Should support printing 'hello world'", () => {
     exitCode: 0,
   });
 });
+
+it("path_open should resolve paths against preopens, not cwd", () => {
+  const tmp = tempDirWithFiles("bun-wasi-test", {
+    "input.txt": "hello from preopens\n",
+  });
+  const testFile = `${tmp}/input.txt`;
+
+  // read-file.wasm: minimal Rust WASI binary (wasm32-wasip1) that reads a file
+  // path from args and prints its contents to stdout.
+  //
+  // Built with:
+  //   cargo init --name read-file-wasi
+  //   # src/main.rs:
+  //   #   use std::{env, fs, process};
+  //   #   fn main() {
+  //   #       let args: Vec<String> = env::args().collect();
+  //   #       if args.len() < 2 { eprintln!("usage: read-file <path>"); process::exit(1); }
+  //   #       match fs::read_to_string(&args[1]) {
+  //   #           Ok(c) => print!("{}", c),
+  //   #           Err(e) => { eprintln!("error: {}: {}", args[1], e); process::exit(1); }
+  //   #       }
+  //   #   }
+  //   cargo build --target wasm32-wasip1 --release
+  const { stdout, stderr, exitCode } = spawnSync({
+    cmd: [bunExe(), import.meta.dir + "/read-file.wasm", testFile],
+    stdout: "pipe",
+    stderr: "pipe",
+    env: bunEnv,
+  });
+
+  expect({
+    stdout: stdout.toString(),
+    stderr: stderr.toString(),
+    exitCode: exitCode,
+  }).toEqual({
+    stdout: "hello from preopens\n",
+    stderr: "",
+    exitCode: 0,
+  });
+});