diff --git a/src/runtime/server/server_body.rs b/src/runtime/server/server_body.rs
index 6bec1cb4814e..132439599c07 100644
--- a/src/runtime/server/server_body.rs
+++ b/src/runtime/server/server_body.rs
@@ -799,6 +799,11 @@ impl AnyRoute {
                         "To mount a directory, make sure the path ends in `/*`"
                     )));
                 }
+                if strings::contains_char(relative_root, 0) {
+                    return Err(global.throw_invalid_arguments(format_args!(
+                        "\"dir\" must not contain null bytes"
+                    )));
+                }
 
                 let style_js = argument.get(global, b"style")?;
                 if style_js.is_none() {
@@ -835,6 +840,30 @@ impl AnyRoute {
                     FrameworkRouter::Style::from_js(style_js.unwrap(), global)?;
                 // Style impls Drop; `?` drops it on the error path.
 
+                {
+                    use bun_sys_jsc::ErrorJsc;
+                    let mut buf = paths::path_buffer_pool::get();
+                    let Some(abs_root) =
+                        paths::resolve_path::join_abs_string_buf_checked::<paths::platform::Auto>(
+                            paths::fs::FileSystem::instance().top_level_dir(),
+                            &mut buf[..],
+                            &[relative_root],
+                        )
+                    else {
+                        let err = sys::Error::from_code(sys::E::ENAMETOOLONG, sys::Tag::open)
+                            .with_path(relative_root);
+                        return Err(global.throw_value(err.to_js(global)?));
+                    };
+                    match sys::open_a(
+                        abs_root,
+                        sys::O::DIRECTORY | sys::O::CLOEXEC | sys::O::RDONLY,
+                        0,
+                    ) {
+                        Ok(fd) => drop(sys::File::from_fd(fd)),
+                        Err(err) => return Err(global.throw_value(err.to_js(global)?)),
+                    }
+                }
+
                 // trim the /*
                 // NOTE: `FileSystemRouterType` fields are `Cow<'static,[u8]>`.
                 // Rather
diff --git a/test/js/bun/http/serve-directory-routes.test.ts b/test/js/bun/http/serve-directory-routes.test.ts
index bd4cd5c85757..8e281b4eaef5 100644
--- a/test/js/bun/http/serve-directory-routes.test.ts
+++ b/test/js/bun/http/serve-directory-routes.test.ts
@@ -529,6 +529,48 @@ describe("Bun.serve() directory routes", () => {
     ).toThrow(expect.objectContaining({ code: "ENOENT" }));
   });
 
+  it("throws if the directory of a { dir, style } mount does not exist", () => {
+    using dir = tempDir("serve-dir-style-enoent", {});
+    expect(() =>
+      serve({
+        port: 0,
+        development: true,
+        routes: { "/*": { dir: join(String(dir), "does-not-exist"), style: "nextjs-pages" } },
+      }),
+    ).toThrow(expect.objectContaining({ code: "ENOENT" }));
+  });
+
+  it("throws if the directory of a { dir, style } mount is a file", () => {
+    using dir = tempDir("serve-dir-style-enotdir", { pages: "not a directory" });
+    expect(() =>
+      serve({
+        port: 0,
+        development: true,
+        routes: { "/*": { dir: join(String(dir), "pages"), style: "nextjs-pages" } },
+      }),
+    ).toThrow(expect.objectContaining({ code: "ENOTDIR" }));
+  });
+
+  it("rejects a dir with an embedded null byte", () => {
+    using dir = tempDir("serve-dir-nul", { "public/x.txt": "x" });
+    const withNul = join(String(dir), "public") + "\0ignored";
+    expect(() => serve({ port: 0, routes: { "/*": { dir: withNul } } })).toThrow(/null bytes/);
+    expect(() =>
+      serve({ port: 0, development: true, routes: { "/*": { dir: withNul, style: "nextjs-pages" } } }),
+    ).toThrow(/null bytes/);
+  });
+
+  it("throws if the directory of a { dir, style } mount is too long for a path", () => {
+    const dir = Buffer.alloc(100_000, "a").toString();
+    expect(() =>
+      serve({
+        port: 0,
+        development: true,
+        routes: { "/*": { dir, style: "nextjs-pages" } },
+      }),
+    ).toThrow(expect.objectContaining({ code: "ENAMETOOLONG" }));
+  });
+
   it("serves correctly with more unique paths than stat-cache slots", async () => {
     const N = 300; // > STAT_CACHE_SLOTS (256)
     const files: Record<string, string> = {};