diff --git a/sys/fs/fuse/fuse_internal.h b/sys/fs/fuse/fuse_internal.h
--- a/sys/fs/fuse/fuse_internal.h
+++ b/sys/fs/fuse/fuse_internal.h
@@ -250,12 +250,12 @@
 struct pseudo_dirent {
 	uint32_t d_namlen;
 };
-int fuse_internal_readdir(struct vnode *vp, struct uio *uio, off_t startoff,
+int fuse_internal_readdir(struct vnode *vp, struct uio *uio,
     struct fuse_filehandle *fufh, struct fuse_iov *cookediov, int *ncookies,
     uint64_t *cookies);
-int fuse_internal_readdir_processdata(struct uio *uio, off_t startoff,
-    int *fnd_start, size_t reqsize, void *buf, size_t bufsize,
-    struct fuse_iov *cookediov, int *ncookies, uint64_t **cookiesp);
+int fuse_internal_readdir_processdata(struct uio *uio, size_t reqsize,
+    void *buf, size_t bufsize, struct fuse_iov *cookediov, int *ncookies,
+    uint64_t **cookiesp);
 
 /* remove */
 
diff --git a/sys/fs/fuse/fuse_internal.c b/sys/fs/fuse/fuse_internal.c
--- a/sys/fs/fuse/fuse_internal.c
+++ b/sys/fs/fuse/fuse_internal.c
@@ -553,7 +553,6 @@
 int
 fuse_internal_readdir(struct vnode *vp,
     struct uio *uio,
-    off_t startoff,
     struct fuse_filehandle *fufh,
     struct fuse_iov *cookediov,
     int *ncookies,
@@ -562,7 +561,6 @@
 	int err = 0;
 	struct fuse_dispatcher fdi;
 	struct fuse_read_in *fri = NULL;
-	int fnd_start;
 
 	if (uio_resid(uio) == 0)
 		return 0;
@@ -572,18 +570,6 @@
 	 * Note that we DO NOT have a UIO_SYSSPACE here (so no need for p2p
 	 * I/O).
 	 */
-
-	/*
-	 * fnd_start is set non-zero once the offset in the directory gets
-	 * to the startoff.  This is done because directories must be read
-	 * from the beginning (offset == 0) when fuse_vnop_readdir() needs
-	 * to do an open of the directory.
-	 * If it is not set non-zero here, it will be set non-zero in
-	 * fuse_internal_readdir_processdata() when uio_offset == startoff.
-	 */
-	fnd_start = 0;
-	if (uio->uio_offset == startoff)
-		fnd_start = 1;
 	while (uio_resid(uio) > 0) {
 		fdi.iosize = sizeof(*fri);
 		fdisp_make_vp(&fdi, FUSE_READDIR, vp, NULL, NULL);
@@ -595,9 +581,8 @@
 
 		if ((err = fdisp_wait_answ(&fdi)))
 			break;
-		if ((err = fuse_internal_readdir_processdata(uio, startoff,
-		    &fnd_start, fri->size, fdi.answ, fdi.iosize, cookediov,
-		    ncookies, &cookies)))
+		if ((err = fuse_internal_readdir_processdata(uio, fri->size,
+			fdi.answ, fdi.iosize, cookediov, ncookies, &cookies)))
 			break;
 	}
 
@@ -612,8 +597,6 @@
  */
 int
 fuse_internal_readdir_processdata(struct uio *uio,
-    off_t startoff,
-    int *fnd_start,
     size_t reqsize,
     void *buf,
     size_t bufsize,
@@ -624,8 +607,6 @@
 	int err = 0;
 	int oreclen;
 	size_t freclen;
-	int ents_copied = 0;
-	int ents_seen = 0;
 
 	struct dirent *de;
 	struct fuse_dirent *fudge;
@@ -636,7 +617,7 @@
 		return -1;
 	for (;;) {
 		if (bufsize < FUSE_NAME_OFFSET) {
-			err = (ents_seen == 0 || ents_copied > 0) ?  -1 : 0;
+			err = -1;
 			break;
 		}
 		fudge = (struct fuse_dirent *)buf;
@@ -647,7 +628,7 @@
 			 * This indicates a partial directory entry at the
 			 * end of the directory data.
 			 */
-			err = (ents_seen == 0 || ents_copied > 0) ?  -1 : 0;
+			err = -1;
 			break;
 		}
 #ifdef ZERO_PAD_INCOMPLETE_BUFS
@@ -669,41 +650,32 @@
 			err = -1;
 			break;
 		}
-		ents_seen++;
-		/*
-		 * Don't start to copy the directory entries out until
-		 * the requested offset in the directory is found.
-		 */
-		if (*fnd_start != 0) {
-			fiov_adjust(cookediov, oreclen);
-			bzero(cookediov->base, oreclen);
-
-			de = (struct dirent *)cookediov->base;
-			de->d_fileno = fudge->ino;
-			de->d_off = fudge->off;
-			de->d_reclen = oreclen;
-			de->d_type = fudge->type;
-			de->d_namlen = fudge->namelen;
-			memcpy((char *)cookediov->base + sizeof(struct dirent) -
-			       MAXNAMLEN - 1,
-			       (char *)buf + FUSE_NAME_OFFSET, fudge->namelen);
-			dirent_terminate(de);
-
-			err = uiomove(cookediov->base, cookediov->len, uio);
-			if (err)
+		fiov_adjust(cookediov, oreclen);
+		bzero(cookediov->base, oreclen);
+
+		de = (struct dirent *)cookediov->base;
+		de->d_fileno = fudge->ino;
+		de->d_off = fudge->off;
+		de->d_reclen = oreclen;
+		de->d_type = fudge->type;
+		de->d_namlen = fudge->namelen;
+		memcpy((char *)cookediov->base + sizeof(struct dirent) -
+		       MAXNAMLEN - 1,
+		       (char *)buf + FUSE_NAME_OFFSET, fudge->namelen);
+		dirent_terminate(de);
+
+		err = uiomove(cookediov->base, cookediov->len, uio);
+		if (err)
+			break;
+		if (cookies != NULL) {
+			if (*ncookies == 0) {
+				err = -1;
 				break;
-			if (cookies != NULL) {
-				if (*ncookies == 0) {
-					err = -1;
-					break;
-				}
-				*cookies = fudge->off;
-				cookies++;
-				(*ncookies)--;
 			}
-			ents_copied++;
-		} else if (startoff == fudge->off)
-			*fnd_start = 1;
+			*cookies = fudge->off;
+			cookies++;
+			(*ncookies)--;
+		}
 		buf = (char *)buf + freclen;
 		bufsize -= freclen;
 		uio_setoffset(uio, fudge->off);
diff --git a/sys/fs/fuse/fuse_vnops.c b/sys/fs/fuse/fuse_vnops.c
--- a/sys/fs/fuse/fuse_vnops.c
+++ b/sys/fs/fuse/fuse_vnops.c
@@ -1846,11 +1846,10 @@
 	struct uio *uio = ap->a_uio;
 	struct ucred *cred = ap->a_cred;
 	struct fuse_filehandle *fufh = NULL;
-	struct fuse_data *mpdata = fuse_get_mpdata(vnode_mount(vp));
+	struct mount *mp = vnode_mount(vp);
 	struct fuse_iov cookediov;
 	int err = 0;
 	uint64_t *cookies;
-	off_t startoff;
 	ssize_t tresid;
 	int ncookies;
 	bool closefufh = false;
@@ -1867,25 +1866,18 @@
 	}
 
 	tresid = uio->uio_resid;
-	startoff = uio->uio_offset;
 	err = fuse_filehandle_get_dir(vp, &fufh, cred, pid);
-	if (err == EBADF && vnode_mount(vp)->mnt_flag & MNT_EXPORTED) {
+	if (err == EBADF && mp->mnt_flag & MNT_EXPORTED) {
+		struct fuse_data *data = fuse_get_mpdata(mp);
+
+		KASSERT(data->dataflags & FSESS_NO_OPENDIR_SUPPORT,
+			("FUSE file systems that don't set "
+			 "FUSE_NO_OPENDIR_SUPPORT should not be exported"));
 		/* 
 		 * nfsd will do VOP_READDIR without first doing VOP_OPEN.  We
-		 * must implicitly open the directory here
+		 * must implicitly open the directory here.
 		 */
 		err = fuse_filehandle_open(vp, FREAD, &fufh, curthread, cred);
-		if (err == 0 && !(mpdata->dataflags & FSESS_NO_OPEN_SUPPORT)) {
-			/*
-			 * FUSE does not require a directory entry's d_off
-			 * field to be valid outside of the lifetime of the
-			 * directory's FUSE file handle.  So we must read the
-			 * directory from the beginning.  However, if the file
-			 * system sets FUSE_NO_OPENDIR_SUPPORT, then the d_off
-			 * field will be valid for the lifetime of the dirent.
-			 */
-			uio->uio_offset = 0;
-		}
 		closefufh = true;
 	}
 	if (err)
@@ -1903,7 +1895,7 @@
 #define DIRCOOKEDSIZE FUSE_DIRENT_ALIGN(FUSE_NAME_OFFSET + MAXNAMLEN + 1)
 	fiov_init(&cookediov, DIRCOOKEDSIZE);
 
-	err = fuse_internal_readdir(vp, uio, startoff, fufh, &cookediov,
+	err = fuse_internal_readdir(vp, uio, fufh, &cookediov,
 		&ncookies, cookies);
 
 	fiov_teardown(&cookediov);
@@ -3108,8 +3100,30 @@
 	struct vattr va;
 	int err;
 
-	if (!(data->dataflags & FSESS_EXPORT_SUPPORT))
+	if (!(data->dataflags & FSESS_EXPORT_SUPPORT)) {
+		/* NFS requires lookups for "." and ".." */
+		SDT_PROBE2(fusefs, , vnops, trace, 1,
+			"VOP_VPTOFH without FUSE_EXPORT_SUPPORT");
 		return EOPNOTSUPP;
+	}
+	if ((mp->mnt_flag & MNT_EXPORTED) &&
+		!(data->dataflags & FSESS_NO_OPENDIR_SUPPORT))
+	{
+		/*
+		 * NFS is stateless, so nfsd must reopen a directory on every
+		 * call to VOP_READDIR, passing in the d_off field from the
+		 * final dirent of the previous invocation.  But without
+		 * FUSE_NO_OPENDIR_SUPPORT, the FUSE protocol does not
+		 * guarantee that d_off will be valid after a directory is
+		 * closed and reopened.  So prohibit exporting FUSE file
+		 * systems that don't set that flag.
+		 *
+		 * But userspace NFS servers don't have this problem.
+                 */
+		SDT_PROBE2(fusefs, , vnops, trace, 1,
+			"VOP_VPTOFH without FUSE_NO_OPENDIR_SUPPORT");
+		return EOPNOTSUPP;
+	}
 
 	err = fuse_internal_getattr(vp, &va, curthread->td_ucred, curthread);
 	if (err)