diff --git a/shell-completion/bash/systemd-run b/shell-completion/bash/systemd-run
index dfcb01231fd..7379431b717 100644
--- a/shell-completion/bash/systemd-run
+++ b/shell-completion/bash/systemd-run
@@ -86,7 +86,7 @@ _systemd_run() {
                          TTYPath= SyslogIdentifier= SyslogLevelPrefix= SyslogLevel=
                          SyslogFacility= TimerSlackNSec= OOMScoreAdjust= ReadWriteDirectories=
                          ReadOnlyDirectories= InaccessibleDirectories= EnvironmentFile=
-                         ProtectSystem= ProtectHome='
+                         ProtectSystem= ProtectHome= RuntimeDirectory='
 
             COMPREPLY=( $(compgen -W '$comps' -- "$cur") )
             return 0
diff --git a/shell-completion/zsh/_systemd-run b/shell-completion/zsh/_systemd-run
index d4fa39341cb..8bb0156a852 100644
--- a/shell-completion/zsh/_systemd-run
+++ b/shell-completion/zsh/_systemd-run
@@ -39,7 +39,7 @@ _arguments \
                 TTYPath= SyslogIdentifier= SyslogLevelPrefix= SyslogLevel= \
                 SyslogFacility= TimerSlackNSec= OOMScoreAdjust= ReadWriteDirectories= \
                 ReadOnlyDirectories= InaccessibleDirectories= EnvironmentFile= \
-                ProtectSystem= ProtectHome= \
+                ProtectSystem= ProtectHome= RuntimeDirectory= \
                 ))' \
         '--description=[Description for unit]:description' \
         '--slice=[Run in the specified slice]:slices:__slices' \
diff --git a/src/core/dbus-execute.c b/src/core/dbus-execute.c
index 04a5a22b72a..db4206a5233 100644
--- a/src/core/dbus-execute.c
+++ b/src/core/dbus-execute.c
@@ -1391,6 +1391,41 @@ int bus_exec_context_set_transient_property(
 
                 return 1;
 
+        } else if (streq(name, "RuntimeDirectory")) {
+                _cleanup_strv_free_ char **l = NULL;
+                char **p;
+
+                r = sd_bus_message_read_strv(message, &l);
+                if (r < 0)
+                        return r;
+
+                STRV_FOREACH(p, l) {
+                        if (!filename_is_valid(*p))
+                                return sd_bus_error_setf(error, SD_BUS_ERROR_INVALID_ARGS, "Runtime directory is not valid %s", *p);
+                }
+
+                if (mode != UNIT_CHECK) {
+                        _cleanup_free_ char *joined = NULL;
+
+                        if (strv_isempty(l)) {
+                                c->runtime_directory = strv_free(c->runtime_directory);
+                                unit_write_drop_in_private_format(u, mode, name, "%s=\n", name);
+                        } else {
+                                r = strv_extend_strv(&c->runtime_directory, l, true);
+
+                                if (r < 0)
+                                        return -ENOMEM;
+
+                                joined = strv_join_quoted(c->runtime_directory);
+                                if (!joined)
+                                        return -ENOMEM;
+
+                                unit_write_drop_in_private_format(u, mode, name, "%s=%s\n", name, joined);
+                        }
+                }
+
+                return 1;
+
         } else if (rlimit_from_string(name) >= 0) {
                 uint64_t rl;
                 rlim_t x;
diff --git a/src/shared/bus-util.c b/src/shared/bus-util.c
index dbae6e7c85e..a13991a9600 100644
--- a/src/shared/bus-util.c
+++ b/src/shared/bus-util.c
@@ -1789,6 +1789,40 @@ int bus_append_unit_property_assignment(sd_bus_message *m, const char *assignmen
 
                 r = sd_bus_message_close_container(m);
 
+        } else if (streq(field, "RuntimeDirectory")) {
+                const char *p;
+
+                r = sd_bus_message_open_container(m, 'v', "as");
+                if (r < 0)
+                        return bus_log_create_error(r);
+
+                r = sd_bus_message_open_container(m, 'a', "s");
+                if (r < 0)
+                        return bus_log_create_error(r);
+
+                p = eq;
+
+                for (;;) {
+                        _cleanup_free_ char *word = NULL;
+
+                        r = extract_first_word(&p, &word, NULL, EXTRACT_QUOTES);
+                        if (r < 0)
+                                return log_error_errno(r, "Failed to parse %s value %s", field, eq);
+
+                        if (r == 0)
+                                break;
+
+                        r = sd_bus_message_append_basic(m, 's', word);
+                        if (r < 0)
+                                return bus_log_create_error(r);
+                }
+
+                r = sd_bus_message_close_container(m);
+                if (r < 0)
+                        return bus_log_create_error(r);
+
+                r = sd_bus_message_close_container(m);
+
         } else {
                 log_error("Unknown assignment %s.", assignment);
                 return -EINVAL;