diff --git a/lib/libc/gen/fdopendir.c b/lib/libc/gen/fdopendir.c
--- a/lib/libc/gen/fdopendir.c
+++ b/lib/libc/gen/fdopendir.c
@@ -30,26 +30,33 @@
  */
 
 #include "namespace.h"
-#include <sys/param.h>
+#include <sys/types.h>
+#include <sys/stat.h>
 
 #include <dirent.h>
 #include <errno.h>
 #include <fcntl.h>
-#include <stdlib.h>
-#include <string.h>
-#include <unistd.h>
+#include <stdbool.h>
 #include "un-namespace.h"
 
 #include "gen-private.h"
 #include "telldir.h"
 
 /*
- * Open a directory with existing file descriptor.
+ * Open a directory with existing file descriptor, which must reference a
+ * directory.
  */
 DIR *
 fdopendir(int fd)
 {
+	struct stat sb;
 
+	if (_fstat(fd, &sb) != 0)
+		return (NULL);
+	if (!S_ISDIR(sb.st_mode)) {
+		errno = ENOTDIR;
+		return (NULL);
+	}
 	if (_fcntl(fd, F_SETFD, FD_CLOEXEC) == -1)
 		return (NULL);
 	return (__opendir_common(fd, DTF_HIDEW | DTF_NODUP, true));
diff --git a/lib/libc/gen/opendir.c b/lib/libc/gen/opendir.c
--- a/lib/libc/gen/opendir.c
+++ b/lib/libc/gen/opendir.c
@@ -30,14 +30,7 @@
  */
 
 #include "namespace.h"
-#include <sys/param.h>
-
 #include <dirent.h>
-#include <errno.h>
-#include <fcntl.h>
-#include <stdlib.h>
-#include <string.h>
-#include <unistd.h>
 #include "un-namespace.h"
 
 #include "gen-private.h"
diff --git a/lib/libc/gen/opendir2.c b/lib/libc/gen/opendir2.c
--- a/lib/libc/gen/opendir2.c
+++ b/lib/libc/gen/opendir2.c
@@ -30,11 +30,12 @@
  */
 
 #include "namespace.h"
-#include <sys/param.h>
+#include <sys/types.h>
 
 #include <dirent.h>
 #include <errno.h>
 #include <fcntl.h>
+#include <stdbool.h>
 #include <stdlib.h>
 #include <string.h>
 #include <unistd.h>
@@ -52,8 +53,7 @@
 
 	if ((flags & (__DTF_READALL | __DTF_SKIPREAD)) != 0)
 		return (NULL);
-	if ((fd = _open(name,
-	    O_RDONLY | O_NONBLOCK | O_DIRECTORY | O_CLOEXEC)) == -1)
+	if ((fd = _open(name, O_DIRECTORY | O_RDONLY | O_CLOEXEC)) == -1)
 		return (NULL);
 
 	dir = __opendir_common(fd, flags, false);
diff --git a/lib/libc/tests/gen/Makefile b/lib/libc/tests/gen/Makefile
--- a/lib/libc/tests/gen/Makefile
+++ b/lib/libc/tests/gen/Makefile
@@ -20,6 +20,7 @@
 ATF_TESTS_C+=		glob_blocks_test
 .endif
 ATF_TESTS_C+=		makecontext_test
+ATF_TESTS_C+=		opendir_test
 ATF_TESTS_C+=		popen_test
 ATF_TESTS_C+=		posix_spawn_test
 ATF_TESTS_C+=		realpath2_test
diff --git a/lib/libc/tests/gen/opendir_test.c b/lib/libc/tests/gen/opendir_test.c
new file mode 100644
--- /dev/null
+++ b/lib/libc/tests/gen/opendir_test.c
@@ -0,0 +1,144 @@
+/*-
+ * Copyright (c) 2025 Klara, Inc.
+ *
+ * SPDX-License-Identifier: BSD-2-Clause
+ */
+
+#include <sys/stat.h>
+
+#include <dirent.h>
+#include <errno.h>
+#include <fcntl.h>
+#include <stdio.h>
+#include <stdlib.h>
+
+#include <atf-c.h>
+
+/*
+ * Create a directory with a single subdirectory.
+ */
+static void
+opendir_prepare(const struct atf_tc *tc)
+{
+	ATF_REQUIRE_EQ(0, mkdir("dir", 0755));
+	ATF_REQUIRE_EQ(0, mkdir("dir/subdir", 0755));
+}
+
+/*
+ * Assuming dirp represents the directory created by opendir_prepare(),
+ * verify that readdir() returns what we expected to see there.
+ */
+static void
+opendir_check(const struct atf_tc *tc, DIR *dirp)
+{
+	struct dirent *ent;
+
+	ATF_REQUIRE((ent = readdir(dirp)) != NULL);
+	ATF_CHECK_EQ(1, ent->d_namlen);
+	ATF_CHECK_STREQ(".", ent->d_name);
+	ATF_CHECK_EQ(DT_DIR, ent->d_type);
+	ATF_REQUIRE((ent = readdir(dirp)) != NULL);
+	ATF_CHECK_EQ(2, ent->d_namlen);
+	ATF_CHECK_STREQ("..", ent->d_name);
+	ATF_CHECK_EQ(DT_DIR, ent->d_type);
+	ATF_REQUIRE((ent = readdir(dirp)) != NULL);
+	ATF_CHECK_EQ(sizeof("subdir") - 1, ent->d_namlen);
+	ATF_CHECK_STREQ("subdir", ent->d_name);
+	ATF_CHECK_EQ(DT_DIR, ent->d_type);
+	ATF_CHECK(readdir(dirp) == NULL);
+}
+
+ATF_TC(opendir_ok);
+ATF_TC_HEAD(opendir_ok, tc)
+{
+	atf_tc_set_md_var(tc, "descr", "Open a directory.");
+}
+ATF_TC_BODY(opendir_ok, tc)
+{
+	DIR *dirp;
+
+	opendir_prepare(tc);
+	ATF_REQUIRE((dirp = opendir("dir")) != NULL);
+	opendir_check(tc, dirp);
+	ATF_CHECK_EQ(0, closedir(dirp));
+}
+
+ATF_TC(opendir_fifo);
+ATF_TC_HEAD(opendir_fifo, tc)
+{
+	atf_tc_set_md_var(tc, "descr", "Do not hang if given a named pipe.");
+}
+ATF_TC_BODY(opendir_fifo, tc)
+{
+	DIR *dirp;
+	int fd;
+
+	ATF_REQUIRE((fd = mkfifo("fifo", 0644)) >= 0);
+	ATF_REQUIRE_EQ(0, close(fd));
+	ATF_REQUIRE((dirp = opendir("fifo")) == NULL);
+	ATF_CHECK_EQ(ENOTDIR, errno);
+}
+
+ATF_TC(fdopendir_ok);
+ATF_TC_HEAD(fdopendir_ok, tc)
+{
+	atf_tc_set_md_var(tc, "descr",
+	    "Open a directory from a directory descriptor.");
+}
+ATF_TC_BODY(fdopendir_ok, tc)
+{
+	DIR *dirp;
+	int dd;
+
+	opendir_prepare(tc);
+	ATF_REQUIRE((dd = open("dir", O_DIRECTORY | O_RDONLY)) >= 0);
+	ATF_REQUIRE((dirp = fdopendir(dd)) != NULL);
+	opendir_check(tc, dirp);
+	ATF_CHECK_EQ(dd, fdclosedir(dirp));
+	ATF_CHECK_EQ(0, close(dd));
+}
+
+ATF_TC(fdopendir_ebadf);
+ATF_TC_HEAD(fdopendir_ebadf, tc)
+{
+	atf_tc_set_md_var(tc, "descr",
+	    "Open a directory from an invalid descriptor.");
+}
+ATF_TC_BODY(fdopendir_ebadf, tc)
+{
+	DIR *dirp;
+	int dd;
+
+	ATF_REQUIRE_EQ(0, mkdir("dir", 0755));
+	ATF_REQUIRE((dd = open("dir", O_DIRECTORY | O_RDONLY)) >= 0);
+	ATF_CHECK_EQ(0, close(dd));
+	ATF_REQUIRE((dirp = fdopendir(dd)) == NULL);
+	ATF_CHECK_EQ(EBADF, errno);
+}
+
+ATF_TC(fdopendir_enotdir);
+ATF_TC_HEAD(fdopendir_enotdir, tc)
+{
+	atf_tc_set_md_var(tc, "descr",
+	    "Open a directory from a non-directory descriptor.");
+}
+ATF_TC_BODY(fdopendir_enotdir, tc)
+{
+	DIR *dirp;
+	int fd;
+
+	ATF_REQUIRE((fd = creat("file", 0644)) >= 0);
+	ATF_REQUIRE((dirp = fdopendir(fd)) == NULL);
+	ATF_CHECK_EQ(ENOTDIR, errno);
+	ATF_CHECK_EQ(0, close(fd));
+}
+
+ATF_TP_ADD_TCS(tp)
+{
+	ATF_TP_ADD_TC(tp, opendir_ok);
+	ATF_TP_ADD_TC(tp, fdopendir_ok);
+	ATF_TP_ADD_TC(tp, fdopendir_ebadf);
+	ATF_TP_ADD_TC(tp, fdopendir_enotdir);
+	ATF_TP_ADD_TC(tp, opendir_fifo);
+	return (atf_no_error());
+}