diff --git a/file.c b/file.c
index 3c71f3303d..0ba6622479 100644
--- a/file.c
+++ b/file.c
@@ -4574,12 +4574,16 @@ rb_check_realpath_internal(VALUE basedir, VALUE path, rb_encoding *origenc, enum
     if (origenc) unresolved_path = TO_OSPATH(unresolved_path);
 
     if ((resolved_ptr = realpath(RSTRING_PTR(unresolved_path), resolved_buffer)) == NULL) {
-        /* glibc realpath(3) does not allow /path/to/file.rb/../other_file.rb,
+        /*
+           wasi-libc 22 and later support realpath(3) but return ENOTSUP
+           when the underlying host syscall returns it.
+           glibc realpath(3) does not allow /path/to/file.rb/../other_file.rb,
            returning ENOTDIR in that case.
            glibc realpath(3) can also return ENOENT for paths that exist,
            such as /dev/fd/5.
            Fallback to the emulated approach in either of those cases. */
-        if (errno == ENOTDIR ||
+        if (errno == ENOTSUP ||
+            errno == ENOTDIR ||
             (errno == ENOENT && rb_file_exist_p(0, unresolved_path))) {
             return rb_check_realpath_emulate(basedir, path, origenc, mode);