diff --git a/src/syscall/fs_wasip1.go b/src/syscall/fs_wasip1.go
index ef04af69660..ab00e5ba22e 100644
--- a/src/syscall/fs_wasip1.go
+++ b/src/syscall/fs_wasip1.go
@@ -100,6 +100,63 @@ const (
 	fullRights  = rights(^uint32(0))
 	readRights  = rights(RIGHT_FD_READ | RIGHT_FD_READDIR)
 	writeRights = rights(RIGHT_FD_DATASYNC | RIGHT_FD_WRITE | RIGHT_FD_ALLOCATE | RIGHT_PATH_FILESTAT_SET_SIZE)
+
+	// Some runtimes have very strict expectations when it comes to which
+	// rights can be enabled on files opened by path_open. The fileRights
+	// constant is used as a mask to retain only bits for operations that
+	// are supported on files.
+	fileRights rights = RIGHT_FD_DATASYNC |
+		RIGHT_FD_READ |
+		RIGHT_FD_SEEK |
+		RIGHT_FDSTAT_SET_FLAGS |
+		RIGHT_FD_SYNC |
+		RIGHT_FD_TELL |
+		RIGHT_FD_WRITE |
+		RIGHT_FD_ADVISE |
+		RIGHT_FD_ALLOCATE |
+		RIGHT_PATH_CREATE_DIRECTORY |
+		RIGHT_PATH_CREATE_FILE |
+		RIGHT_PATH_LINK_SOURCE |
+		RIGHT_PATH_LINK_TARGET |
+		RIGHT_PATH_OPEN |
+		RIGHT_FD_READDIR |
+		RIGHT_PATH_READLINK |
+		RIGHT_PATH_RENAME_SOURCE |
+		RIGHT_PATH_RENAME_TARGET |
+		RIGHT_PATH_FILESTAT_GET |
+		RIGHT_PATH_FILESTAT_SET_SIZE |
+		RIGHT_PATH_FILESTAT_SET_TIMES |
+		RIGHT_FD_FILESTAT_GET |
+		RIGHT_FD_FILESTAT_SET_SIZE |
+		RIGHT_FD_FILESTAT_SET_TIMES |
+		RIGHT_PATH_SYMLINK |
+		RIGHT_PATH_REMOVE_DIRECTORY |
+		RIGHT_PATH_UNLINK_FILE |
+		RIGHT_POLL_FD_READWRITE
+
+	// Runtimes like wasmtime and wasmedge will refuse to open directories
+	// if the rights requested by the application exceed the operations that
+	// can be performed on a directory.
+	dirRights rights = RIGHT_FD_SEEK |
+		RIGHT_FDSTAT_SET_FLAGS |
+		RIGHT_FD_SYNC |
+		RIGHT_PATH_CREATE_DIRECTORY |
+		RIGHT_PATH_CREATE_FILE |
+		RIGHT_PATH_LINK_SOURCE |
+		RIGHT_PATH_LINK_TARGET |
+		RIGHT_PATH_OPEN |
+		RIGHT_FD_READDIR |
+		RIGHT_PATH_READLINK |
+		RIGHT_PATH_RENAME_SOURCE |
+		RIGHT_PATH_RENAME_TARGET |
+		RIGHT_PATH_FILESTAT_GET |
+		RIGHT_PATH_FILESTAT_SET_SIZE |
+		RIGHT_PATH_FILESTAT_SET_TIMES |
+		RIGHT_FD_FILESTAT_GET |
+		RIGHT_FD_FILESTAT_SET_TIMES |
+		RIGHT_PATH_SYMLINK |
+		RIGHT_PATH_REMOVE_DIRECTORY |
+		RIGHT_PATH_UNLINK_FILE
 )
 
 // https://github.com/WebAssembly/WASI/blob/a2b96e81c0586125cc4dc79a5be0b78d9a059925/legacy/preview1/docs.md#-fd_closefd-fd---result-errno
@@ -435,11 +492,11 @@ func Open(path string, openmode int, perm uint32) (int, error) {
 	var rights rights
 	switch openmode & (O_RDONLY | O_WRONLY | O_RDWR) {
 	case O_RDONLY:
-		rights = fullRights & ^writeRights
+		rights = fileRights & ^writeRights
 	case O_WRONLY:
-		rights = fullRights & ^readRights
+		rights = fileRights & ^readRights
 	case O_RDWR:
-		rights = fullRights
+		rights = fileRights
 	}
 
 	var fdflags fdflags
@@ -458,10 +515,32 @@ func Open(path string, openmode int, perm uint32) (int, error) {
 		pathLen,
 		oflags,
 		rights,
-		fullRights,
+		fileRights,
 		fdflags,
 		unsafe.Pointer(&fd),
 	)
+	if errno == EISDIR && oflags == 0 && fdflags == 0 && ((rights & writeRights) == 0) {
+		// wasmtime and wasmedge will error if attempting to open a directory
+		// because we are asking for too many rights. However, we cannot
+		// determine ahread of time if the path we are about to open is a
+		// directory, so instead we fallback to a second call to path_open with
+		// a more limited set of rights.
+		//
+		// This approach is subject to a race if the file system is modified
+		// concurrently, so we also inject OFLAG_DIRECTORY to ensure that we do
+		// not accidentally open a file which is not a directory.
+		errno = path_open(
+			dirFd,
+			LOOKUP_SYMLINK_FOLLOW,
+			pathPtr,
+			pathLen,
+			oflags|OFLAG_DIRECTORY,
+			rights&dirRights,
+			fileRights,
+			fdflags,
+			unsafe.Pointer(&fd),
+		)
+	}
 	return int(fd), errnoErr(errno)
 }