diff --git a/lib/libvmmapi/vmmapi.h b/lib/libvmmapi/vmmapi.h
--- a/lib/libvmmapi/vmmapi.h
+++ b/lib/libvmmapi/vmmapi.h
@@ -115,6 +115,7 @@
 struct vmctx *vm_open(const char *name);
 #define	VMMAPI_OPEN_CREATE	0x01	/* create if the VM does not exist */
 #define	VMMAPI_OPEN_REINIT	0x02	/* reinitialize the VM if it exists */
+#define	VMMAPI_OPEN_CREATE_DESTROY_ON_CLOSE	0x04	/* Destroy the VM when closing vmm_ctl */
 struct vmctx *vm_openf(const char *name, int flags);
 void	vm_close(struct vmctx *ctx);
 void	vm_destroy(struct vmctx *ctx);
diff --git a/lib/libvmmapi/vmmapi.c b/lib/libvmmapi/vmmapi.c
--- a/lib/libvmmapi/vmmapi.c
+++ b/lib/libvmmapi/vmmapi.c
@@ -100,11 +100,13 @@
 }
 
 static int
-vm_ctl_create(const char *name, int ctlfd)
+vm_ctl_create(const char *name, int flags, int ctlfd)
 {
 	struct vmmctl_vm_create vmc;
 
 	memset(&vmc, 0, sizeof(vmc));
+	if ((flags & VMMAPI_OPEN_CREATE_DESTROY_ON_CLOSE) != 0)
+		vmc.flags |= VMMCTL_CREATE_DESTROY_ON_CLOSE;
 	if (strlcpy(vmc.name, name, sizeof(vmc.name)) >= sizeof(vmc.name)) {
 		errno = ENAMETOOLONG;
 		return (-1);
@@ -121,7 +123,7 @@
 	if (fd < 0)
 		return (-1);
 
-	error = vm_ctl_create(name, fd);
+	error = vm_ctl_create(name, 0, fd);
 	if (error != 0) {
 		error = errno;
 		(void)close(fd);
@@ -162,7 +164,7 @@
 	vm->fd = vm_device_open(vm->name);
 	if (vm->fd < 0 && errno == ENOENT) {
 		if (flags & VMMAPI_OPEN_CREATE) {
-			if (vm_ctl_create(vm->name, vm->ctlfd) != 0)
+			if (vm_ctl_create(vm->name, flags, vm->ctlfd) != 0)
 				goto err;
 			vm->fd = vm_device_open(vm->name);
 			created = true;
diff --git a/sys/dev/vmm/vmm_dev.h b/sys/dev/vmm/vmm_dev.h
--- a/sys/dev/vmm/vmm_dev.h
+++ b/sys/dev/vmm/vmm_dev.h
@@ -70,9 +70,13 @@
 
 #endif /* _KERNEL */
 
+#define VMMCTL_CREATE_DESTROY_ON_CLOSE 0x1
+#define VMMCTL_FLAGS_MASK	       (VMMCTL_CREATE_DESTROY_ON_CLOSE)
+
 struct vmmctl_vm_create {
 	char name[VM_MAX_NAMELEN + 1];
-	int reserved[16];
+	uint32_t flags;
+	int reserved[15];
 };
 
 struct vmmctl_vm_destroy {
diff --git a/sys/dev/vmm/vmm_dev.c b/sys/dev/vmm/vmm_dev.c
--- a/sys/dev/vmm/vmm_dev.c
+++ b/sys/dev/vmm/vmm_dev.c
@@ -77,10 +77,15 @@
 	struct cdev	*cdev;
 	struct ucred	*ucred;
 	SLIST_ENTRY(vmmdev_softc) link;
+	LIST_ENTRY(vmmdev_softc) priv_link;
 	SLIST_HEAD(, devmem_softc) devmem;
 	int		flags;
 };
 
+struct vmmctl_priv {
+	LIST_HEAD(, vmmdev_softc) softcs;
+};
+
 static bool vmm_initialized = false;
 
 static SLIST_HEAD(, vmmdev_softc) head;
@@ -103,6 +108,7 @@
 
 static void devmem_destroy(void *arg);
 static int devmem_create_cdev(struct vmmdev_softc *sc, int id, char *devmem);
+static void vmmdev_destroy(struct vmmdev_softc *sc);
 
 static int
 vmm_priv_check(struct ucred *ucred)
@@ -910,6 +916,8 @@
 
 	sx_xlock(&vmmdev_mtx);
 	SLIST_REMOVE(&head, sc, vmmdev_softc, link);
+	if ((sc->flags & VMMCTL_CREATE_DESTROY_ON_CLOSE) != 0)
+		LIST_REMOVE(sc, priv_link);
 	sx_xunlock(&vmmdev_mtx);
 	free(sc, M_VMMDEV);
 }
@@ -988,17 +996,23 @@
 }
 
 static int
-vmmdev_create(const char *name, struct ucred *cred)
+vmmdev_create(const char *name, uint32_t flags, struct ucred *cred)
 {
 	struct make_dev_args mda;
 	struct cdev *cdev;
 	struct vmmdev_softc *sc;
+	struct vmmctl_priv *priv;
 	struct vm *vm;
 	int error;
 
 	if (name == NULL || strlen(name) > VM_MAX_NAMELEN)
 		return (EINVAL);
 
+	flags &= VMMCTL_FLAGS_MASK;
+	error = devfs_get_cdevpriv((void **)&priv);
+	if (error)
+		return (error);
+
 	sx_xlock(&vmmdev_mtx);
 	sc = vmmdev_lookup(name, cred);
 	if (sc != NULL) {
@@ -1018,6 +1032,9 @@
 	}
 	sc = vmmdev_alloc(vm, cred);
 	SLIST_INSERT_HEAD(&head, sc, link);
+	sc->flags = flags;
+	if ((flags & VMMCTL_CREATE_DESTROY_ON_CLOSE) != 0)
+		LIST_INSERT_HEAD(&priv->softcs, sc, priv_link);
 
 	make_dev_args_init(&mda);
 	mda.mda_devsw = &vmmdevsw;
@@ -1055,7 +1072,7 @@
 	buf = malloc(buflen, M_VMMDEV, M_WAITOK | M_ZERO);
 	error = sysctl_handle_string(oidp, buf, buflen, req);
 	if (error == 0 && req->newptr != NULL)
-		error = vmmdev_create(buf, req->td->td_ucred);
+		error = vmmdev_create(buf, 0, req->td->td_ucred);
 	free(buf, M_VMMDEV);
 	return (error);
 }
@@ -1064,10 +1081,49 @@
     NULL, 0, sysctl_vmm_create, "A",
     "Create a vmm(4) instance (legacy interface)");
 
+static void
+vmmctl_dtor(void *arg)
+{
+	struct cdev *sc_cdev;
+	struct vmmdev_softc *sc;
+	struct vmmctl_priv *priv = arg;
+
+	/*
+	 * Scan the softc list for any VMs associated with
+	 * the current descriptor and destroy them.
+	 */
+	sx_xlock(&vmmdev_mtx);
+	while (!LIST_EMPTY(&priv->softcs)) {
+		sc = LIST_FIRST(&priv->softcs);
+		sc_cdev = sc->cdev;
+		if (sc_cdev != NULL) {
+			sc->cdev = NULL;
+		} else {
+			/*
+			 * Another thread has already
+			 * started the removal process.
+			 */
+		}
+		/* Temporarily drop the lock to allow vmmdev_destroy to run. */
+		sx_xunlock(&vmmdev_mtx);
+		if (sc_cdev != NULL) {
+			vm_suspend(sc->vm, VM_SUSPEND_DESTROY);
+			destroy_dev(sc_cdev);
+			/* vmmdev_destroy will unlink the 'priv_link' entry. */
+			vmmdev_destroy(sc);
+		}
+		sx_xlock(&vmmdev_mtx);
+	}
+	sx_xunlock(&vmmdev_mtx);
+
+	free(priv, M_VMMDEV);
+}
+
 static int
 vmmctl_open(struct cdev *cdev, int flags, int fmt, struct thread *td)
 {
 	int error;
+	struct vmmctl_priv *priv;
 
 	error = vmm_priv_check(td->td_ucred);
 	if (error != 0)
@@ -1076,6 +1132,14 @@
 	if ((flags & FWRITE) == 0)
 		return (EPERM);
 
+	priv = malloc(sizeof(*priv), M_VMMDEV, M_WAITOK | M_ZERO);
+	LIST_INIT(&priv->softcs);
+	error = devfs_set_cdevpriv(priv, vmmctl_dtor);
+	if (error != 0) {
+		free(priv, M_VMMDEV);
+		return (error);
+	}
+
 	return (0);
 }
 
@@ -1098,7 +1162,7 @@
 			}
 		}
 
-		error = vmmdev_create(vmc->name, td->td_ucred);
+		error = vmmdev_create(vmc->name, vmc->flags, td->td_ucred);
 		break;
 	}
 	case VMMCTL_VM_DESTROY: {