diff --git a/NEWS b/NEWS
index 8f6f77c70d..cc640eaa3d 100644
--- a/NEWS
+++ b/NEWS
@@ -46,6 +46,9 @@ CHANGES WITH 258 in spe:
           owned by a non-system user/group. It is recommended to check udev
           rules files with 'udevadm verify' and/or 'udevadm test' commands if
           the specified user/group in OWNER=/GROUP= are valid.
+          Similarly, systemd-networkd refuses User=/Group= settings with a
+          non-system user/group specified in .netdev files for Tun/Tap
+          interfaces.
 
         * systemd-cryptenroll, systemd-repart and systemd-creds no longer
           default to locking TPM2 enrollments to the current, literal value of
diff --git a/man/systemd.netdev.xml b/man/systemd.netdev.xml
index 9ea59a7763..3bfaf7c215 100644
--- a/man/systemd.netdev.xml
+++ b/man/systemd.netdev.xml
@@ -1970,16 +1970,16 @@ Ports=eth2</programlisting>
       </varlistentry>
       <varlistentry>
         <term><varname>User=</varname></term>
-        <listitem><para>User to grant access to the
-        <filename>/dev/net/tun</filename> device.</para>
+        <listitem><para>User to grant access to the <filename>/dev/net/tun</filename> device. The specified
+        user must be a system user.</para>
 
         <xi:include href="version-info.xml" xpointer="v215"/>
         </listitem>
       </varlistentry>
       <varlistentry>
         <term><varname>Group=</varname></term>
-        <listitem><para>Group to grant access to the
-        <filename>/dev/net/tun</filename> device.</para>
+        <listitem><para>Group to grant access to the <filename>/dev/net/tun</filename> device. The specified
+        group must be a system group.</para>
 
         <xi:include href="version-info.xml" xpointer="v215"/>
         </listitem>
diff --git a/src/network/netdev/tuntap.c b/src/network/netdev/tuntap.c
index 2d96682ca5..48bc007970 100644
--- a/src/network/netdev/tuntap.c
+++ b/src/network/netdev/tuntap.c
@@ -10,13 +10,14 @@
 #include <sys/types.h>
 
 #include "alloc-util.h"
+#include "bitfield.h"
 #include "daemon-util.h"
 #include "fd-util.h"
 #include "networkd-link.h"
 #include "networkd-manager.h"
 #include "socket-util.h"
 #include "tuntap.h"
-#include "user-util.h"
+#include "userdb.h"
 
 #define TUN_DEV "/dev/net/tun"
 
@@ -174,31 +175,14 @@ static int netdev_create_tuntap(NetDev *netdev) {
                         return log_netdev_error_errno(netdev, errno, "TUNSETQUEUE failed: %m");
         }
 
-        if (t->user_name) {
-                const char *user = t->user_name;
-                uid_t uid;
-
-                r = get_user_creds(&user, &uid, NULL, NULL, NULL, USER_CREDS_ALLOW_MISSING);
-                if (r < 0)
-                        return log_netdev_error_errno(netdev, r, "Cannot resolve user name %s: %m", t->user_name);
-
-                if (ioctl(fd, TUNSETOWNER, uid) < 0)
+        if (t->uid != 0)
+                if (ioctl(fd, TUNSETOWNER, t->uid) < 0)
                         return log_netdev_error_errno(netdev, errno, "TUNSETOWNER failed: %m");
-        }
 
-        if (t->group_name) {
-                const char *group = t->group_name;
-                gid_t gid;
-
-                r = get_group_creds(&group, &gid, USER_CREDS_ALLOW_MISSING);
-                if (r < 0)
-                        return log_netdev_error_errno(netdev, r, "Cannot resolve group name %s: %m", t->group_name);
-
-                if (ioctl(fd, TUNSETGROUP, gid) < 0)
+        if (t->gid != 0)
+                if (ioctl(fd, TUNSETGROUP, t->gid) < 0)
                         return log_netdev_error_errno(netdev, errno, "TUNSETGROUP failed: %m");
 
-        }
-
         if (ioctl(fd, TUNSETPERSIST, 1) < 0)
                 return log_netdev_error_errno(netdev, errno, "TUNSETPERSIST failed: %m");
 
@@ -226,6 +210,9 @@ static void tuntap_done(NetDev *netdev) {
 }
 
 static int tuntap_verify(NetDev *netdev, const char *filename) {
+        TunTap *t = TUNTAP(netdev);
+        int r;
+
         assert(netdev);
 
         if (netdev->mtu != 0)
@@ -240,6 +227,36 @@ static int tuntap_verify(NetDev *netdev, const char *filename) {
                                    "Please set it in the corresponding .network file.",
                                    netdev_kind_to_string(netdev->kind), filename);
 
+        if (t->user_name) {
+                _cleanup_(user_record_unrefp) UserRecord *ur = NULL;
+                UserDBMatch match = USERDB_MATCH_NULL;
+
+                match.disposition_mask = INDEX_TO_MASK(uint64_t, USER_SYSTEM);
+
+                r = userdb_by_name(t->user_name, &match, USERDB_PARSE_NUMERIC, &ur);
+                if (r == -ENOEXEC)
+                        log_netdev_warning_errno(netdev, r, "User %s is not a system user, ignoring.", t->user_name);
+                else if (r < 0)
+                        log_netdev_warning_errno(netdev, r, "Cannot resolve user name %s, ignoring: %m", t->user_name);
+                else
+                        t->uid = ur->uid;
+        }
+
+        if (t->group_name) {
+                _cleanup_(group_record_unrefp) GroupRecord *gr = NULL;
+                UserDBMatch match = USERDB_MATCH_NULL;
+
+                match.disposition_mask = INDEX_TO_MASK(uint64_t, USER_SYSTEM);
+
+                r = groupdb_by_name(t->group_name, &match, USERDB_PARSE_NUMERIC, &gr);
+                if (r == -ENOEXEC)
+                        log_netdev_warning_errno(netdev, r, "Group %s is not a system group, ignoring.", t->group_name);
+                else if (r < 0)
+                        log_netdev_warning_errno(netdev, r, "Cannot resolve group name %s, ignoring: %m", t->group_name);
+                else
+                        t->gid = gr->gid;
+        }
+
         return 0;
 }
 
diff --git a/src/network/netdev/tuntap.h b/src/network/netdev/tuntap.h
index e2de8eb6bb..f345548f95 100644
--- a/src/network/netdev/tuntap.h
+++ b/src/network/netdev/tuntap.h
@@ -1,20 +1,21 @@
 /* SPDX-License-Identifier: LGPL-2.1-or-later */
 #pragma once
 
-typedef struct TunTap TunTap;
-
 #include "netdev.h"
+#include "user-util.h"
 
-struct TunTap {
+typedef struct TunTap {
         NetDev meta;
 
         char *user_name;
+        uid_t uid;
         char *group_name;
+        gid_t gid;
         bool multi_queue;
         bool packet_info;
         bool vnet_hdr;
         bool keep_fd;
-};
+} TunTap;
 
 DEFINE_NETDEV_CAST(TUN, TunTap);
 DEFINE_NETDEV_CAST(TAP, TunTap);