diff --git a/crates/test-programs/README.md b/crates/test-programs/README.md
index 662216f426..31f3c1bfad 100644
--- a/crates/test-programs/README.md
+++ b/crates/test-programs/README.md
@@ -1,2 +1,7 @@
 This is the `test-programs` crate, which builds and runs whole programs
 compiled to wasm32-wasi.
+
+To actually run these tests, the test-programs feature must be enabled, e.g.:
+```
+cargo test --features test-programs/test_programs --package test-programs
+```
diff --git a/crates/test-programs/wasi-tests/src/bin/path_open_missing.rs b/crates/test-programs/wasi-tests/src/bin/path_open_missing.rs
new file mode 100644
index 0000000000..410b602c45
--- /dev/null
+++ b/crates/test-programs/wasi-tests/src/bin/path_open_missing.rs
@@ -0,0 +1,43 @@
+use std::{env, process};
+use wasi_tests::{open_scratch_directory};
+
+unsafe fn test_path_open_missing(dir_fd: wasi::Fd) {
+    assert_eq!(
+        wasi::path_open(
+            dir_fd,
+            0,
+            "file",
+            0, // not passing O_CREAT here
+            0,
+            0,
+            0,
+        )
+        .expect_err("trying to open a file that doesn't exist")
+        .raw_error(),
+        wasi::ERRNO_NOENT,
+        "errno should be ERRNO_NOENT"
+    );
+}
+
+fn main() {
+    let mut args = env::args();
+    let prog = args.next().unwrap();
+    let arg = if let Some(arg) = args.next() {
+        arg
+    } else {
+        eprintln!("usage: {} <scratch directory>", prog);
+        process::exit(1);
+    };
+
+    // Open scratch directory
+    let dir_fd = match open_scratch_directory(&arg) {
+        Ok(dir_fd) => dir_fd,
+        Err(err) => {
+            eprintln!("{}", err);
+            process::exit(1)
+        }
+    };
+
+    // Run the tests.
+    unsafe { test_path_open_missing(dir_fd) }
+}
diff --git a/crates/wasi-common/src/virtfs.rs b/crates/wasi-common/src/virtfs.rs
index 0023825208..8eba9808e6 100644
--- a/crates/wasi-common/src/virtfs.rs
+++ b/crates/wasi-common/src/virtfs.rs
@@ -661,23 +661,30 @@ impl Handle for VirtualDir {
                 e.get().try_clone().map_err(Into::into)
             }
             Entry::Vacant(v) => {
-                if self.writable {
-                    // Enforce a hard limit at `u32::MAX - 2` files.
-                    // This is to have a constant limit (rather than target-dependent limit we
-                    // would have with `usize`. The limit is the full `u32` range minus two so we
-                    // can reserve "self" and "parent" cookie values.
-                    if entry_count >= (std::u32::MAX - RESERVED_ENTRY_COUNT) as usize {
-                        return Err(Error::Nospc);
+                if oflags.contains(&Oflags::CREAT) {
+                    if self.writable {
+                        // Enforce a hard limit at `u32::MAX - 2` files.
+                        // This is to have a constant limit (rather than target-dependent limit we
+                        // would have with `usize`. The limit is the full `u32` range minus two so we
+                        // can reserve "self" and "parent" cookie values.
+                        if entry_count >= (std::u32::MAX - RESERVED_ENTRY_COUNT) as usize {
+                            return Err(Error::Nospc);
+                        }
+
+                        tracing::trace!(
+                            "VirtualDir::openat creating an InMemoryFile named {}",
+                            path
+                        );
+
+                        let file = Box::new(InMemoryFile::memory_backed());
+                        file.fd_flags.set(fd_flags);
+                        file.set_parent(Some(self.try_clone().expect("can clone self")));
+                        v.insert(file).try_clone().map_err(Into::into)
+                    } else {
+                        Err(Error::Acces)
                     }
-
-                    tracing::trace!("VirtualDir::openat creating an InMemoryFile named {}", path);
-
-                    let file = Box::new(InMemoryFile::memory_backed());
-                    file.fd_flags.set(fd_flags);
-                    file.set_parent(Some(self.try_clone().expect("can clone self")));
-                    v.insert(file).try_clone().map_err(Into::into)
                 } else {
-                    Err(Error::Acces)
+                    Err(Error::Noent)
                 }
             }
         }