diff --git a/man/systemd.netdev.xml b/man/systemd.netdev.xml
index 10397402a46..1836b5fe00e 100644
--- a/man/systemd.netdev.xml
+++ b/man/systemd.netdev.xml
@@ -1241,7 +1241,7 @@
       <varlistentry>
         <term><varname>PrivateKeyFile=</varname></term>
         <listitem>
-          <para>Takes a absolute path to a file which contains the Base64 encoded private key for the interface.
+          <para>Takes an absolute path to a file which contains the Base64 encoded private key for the interface.
           When this option is specified, then <varname>PrivateKey=</varname> is ignored.
           Note that the file must be readable by the user <literal>systemd-network</literal>, so it
           should be, e.g., owned by <literal>root:systemd-network</literal> with a
@@ -1296,6 +1296,16 @@
             with a <literal>0640</literal> file mode.</para>
         </listitem>
       </varlistentry>
+      <varlistentry>
+        <term><varname>PresharedKeyFile=</varname></term>
+        <listitem>
+          <para>Takes an absolute path to a file which contains the Base64 encoded preshared key for the
+          peer. When this option is specified, then <varname>PresharedKey=</varname> is ignored.
+          Note that the file must be readable by the user <literal>systemd-network</literal>, so it
+          should be, e.g., owned by <literal>root:systemd-network</literal> with a
+          <literal>0640</literal> file mode.</para>
+        </listitem>
+      </varlistentry>
       <varlistentry>
         <term><varname>AllowedIPs=</varname></term>
         <listitem>
diff --git a/src/network/netdev/netdev-gperf.gperf b/src/network/netdev/netdev-gperf.gperf
index fcd2ec2097b..1a3d6caeb9f 100644
--- a/src/network/netdev/netdev-gperf.gperf
+++ b/src/network/netdev/netdev-gperf.gperf
@@ -187,4 +187,5 @@ WireGuardPeer.AllowedIPs,          config_parse_wireguard_allowed_ips,   0,
 WireGuardPeer.Endpoint,            config_parse_wireguard_endpoint,      0,                             0
 WireGuardPeer.PublicKey,           config_parse_wireguard_public_key,    0,                             0
 WireGuardPeer.PresharedKey,        config_parse_wireguard_preshared_key, 0,                             0
+WireGuardPeer.PresharedKeyFile,    config_parse_wireguard_preshared_key_file, 0,                        0
 WireGuardPeer.PersistentKeepalive, config_parse_wireguard_keepalive,     0,                             0
diff --git a/src/network/netdev/wireguard.c b/src/network/netdev/wireguard.c
index d897090f722..0b618962015 100644
--- a/src/network/netdev/wireguard.c
+++ b/src/network/netdev/wireguard.c
@@ -53,6 +53,7 @@ static void wireguard_peer_free(WireguardPeer *peer) {
 
         free(peer->endpoint_host);
         free(peer->endpoint_port);
+        free(peer->preshared_key_file);
         explicit_bzero_safe(peer->preshared_key, WG_KEY_LEN);
 
         free(peer);
@@ -602,6 +603,49 @@ int config_parse_wireguard_preshared_key(
         return 0;
 }
 
+int config_parse_wireguard_preshared_key_file(
+                const char *unit,
+                const char *filename,
+                unsigned line,
+                const char *section,
+                unsigned section_line,
+                const char *lvalue,
+                int ltype,
+                const char *rvalue,
+                void *data,
+                void *userdata) {
+
+        _cleanup_(wireguard_peer_free_or_set_invalidp) WireguardPeer *peer = NULL;
+        _cleanup_free_ char *path = NULL;
+        Wireguard *w;
+        int r;
+
+        assert(data);
+        w = WIREGUARD(data);
+        assert(w);
+
+        r = wireguard_peer_new_static(w, filename, section_line, &peer);
+        if (r < 0)
+                return r;
+
+        if (isempty(rvalue)) {
+                peer->preshared_key_file = mfree(peer->preshared_key_file);
+                TAKE_PTR(peer);
+                return 0;
+        }
+
+        path = strdup(rvalue);
+        if (!path)
+                return log_oom();
+
+        if (path_simplify_and_warn(path, PATH_CHECK_ABSOLUTE, unit, filename, line, lvalue) < 0)
+                return 0;
+
+        free_and_replace(peer->preshared_key_file, path);
+        TAKE_PTR(peer);
+        return 0;
+}
+
 int config_parse_wireguard_public_key(
                 const char *unit,
                 const char *filename,
@@ -879,6 +923,7 @@ finalize:
 
 static int wireguard_peer_verify(WireguardPeer *peer) {
         NetDev *netdev = NETDEV(peer->wireguard);
+        int r;
 
         if (section_is_invalid(peer->section))
                 return -EINVAL;
@@ -889,6 +934,14 @@ static int wireguard_peer_verify(WireguardPeer *peer) {
                                               "Ignoring [WireGuardPeer] section from line %u.",
                                               peer->section->filename, peer->section->line);
 
+        r = wireguard_read_key_file(peer->preshared_key_file, peer->preshared_key);
+        if (r < 0)
+                return log_netdev_error_errno(netdev, r,
+                                              "%s: Failed to read preshared key from '%s'. "
+                                              "Ignoring [WireGuardPeer] section from line %u.",
+                                              peer->section->filename, peer->preshared_key_file,
+                                              peer->section->line);
+
         return 0;
 }
 
diff --git a/src/network/netdev/wireguard.h b/src/network/netdev/wireguard.h
index 6cf6eec14db..4ae520c52ba 100644
--- a/src/network/netdev/wireguard.h
+++ b/src/network/netdev/wireguard.h
@@ -21,6 +21,7 @@ typedef struct WireguardPeer {
 
         uint8_t public_key[WG_KEY_LEN];
         uint8_t preshared_key[WG_KEY_LEN];
+        char *preshared_key_file;
         uint32_t flags;
         uint16_t persistent_keepalive_interval;
 
@@ -63,4 +64,5 @@ CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_public_key);
 CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_private_key);
 CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_private_key_file);
 CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_preshared_key);
+CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_preshared_key_file);
 CONFIG_PARSER_PROTOTYPE(config_parse_wireguard_keepalive);
diff --git a/test/fuzz/fuzz-netdev-parser/directives.netdev b/test/fuzz/fuzz-netdev-parser/directives.netdev
index e0756dc7554..7da3955af6b 100644
--- a/test/fuzz/fuzz-netdev-parser/directives.netdev
+++ b/test/fuzz/fuzz-netdev-parser/directives.netdev
@@ -52,6 +52,7 @@ Name=
 [WireGuardPeer]
 Endpoint=
 PresharedKey=
+PresharedKeyFile=
 PersistentKeepalive=
 PublicKey=
 AllowedIPs=