diff --git a/src/journal/journald-server.c b/src/journal/journald-server.c
index d7c8095d79..cfa4b5ffbf 100644
--- a/src/journal/journald-server.c
+++ b/src/journal/journald-server.c
@@ -1353,6 +1353,10 @@ finish:
         if (s->system_journal)
                 journal_file_post_change(s->system_journal);
 
+        /* Save parent directories of runtime journals before closing runtime journals. */
+        _cleanup_strv_free_ char **dirs = NULL;
+        (void) journal_get_directories(j, &dirs);
+
         /* First, close all runtime journals opened in the above. */
         sd_journal_close(j);
 
@@ -1360,9 +1364,19 @@ finish:
         s->runtime_journal = journal_file_offline_close(s->runtime_journal);
 
         /* Remove the runtime directory if the all entries are successfully flushed to /var/. */
-        if (r >= 0)
+        if (r >= 0) {
                 (void) rm_rf(s->runtime_storage.path, REMOVE_ROOT);
 
+                /* The initrd may have a different machine ID from the host's one. Typically, that happens
+                 * when our tests running on qemu, as the host's initrd is picked as is without updating
+                 * the machine ID in the initrd with the one used in the image. Even in such the case, the
+                 * runtime journals in the subdirectory named with the initrd's machine ID are flushed to
+                 * the persistent journal. To make not the runtime journal flushed multiple times, let's
+                 * also remove the runtime directories. */
+                STRV_FOREACH(p, dirs)
+                        (void) rm_rf(*p, REMOVE_ROOT);
+        }
+
         server_driver_message(s, 0, NULL,
                               LOG_MESSAGE("Time spent on flushing to %s is %s for %u entries.",
                                           s->system_storage.path,
diff --git a/src/libsystemd/sd-journal/journal-internal.h b/src/libsystemd/sd-journal/journal-internal.h
index 259aac847d..85d5d32f96 100644
--- a/src/libsystemd/sd-journal/journal-internal.h
+++ b/src/libsystemd/sd-journal/journal-internal.h
@@ -128,6 +128,7 @@ struct sd_journal {
 
 char *journal_make_match_string(sd_journal *j);
 void journal_print_header(sd_journal *j);
+int journal_get_directories(sd_journal *j, char ***ret);
 
 #define JOURNAL_FOREACH_DATA_RETVAL(j, data, l, retval)                     \
         for (sd_journal_restart_data(j); ((retval) = sd_journal_enumerate_data((j), &(data), &(l))) > 0; )
diff --git a/src/libsystemd/sd-journal/sd-journal.c b/src/libsystemd/sd-journal/sd-journal.c
index 6b9ff0a4ed..6e33c06d63 100644
--- a/src/libsystemd/sd-journal/sd-journal.c
+++ b/src/libsystemd/sd-journal/sd-journal.c
@@ -1494,6 +1494,41 @@ error:
         return r;
 }
 
+int journal_get_directories(sd_journal *j, char ***ret) {
+        _cleanup_strv_free_ char **paths = NULL;
+        JournalFile *f;
+        const char *p;
+        size_t n = SIZE_MAX;
+        int r;
+
+        assert(j);
+        assert(ret);
+
+        /* This returns parent directories of opened journal files. */
+
+        ORDERED_HASHMAP_FOREACH_KEY(f, p, j->files) {
+                _cleanup_free_ char *d = NULL;
+
+                /* Ignore paths generated from fd. */
+                if (path_startswith(p, "/proc/"))
+                        continue;
+
+                r = path_extract_directory(p, &d);
+                if (r < 0)
+                        return r;
+
+                if (path_strv_contains(paths, d))
+                        continue;
+
+                r = strv_extend_with_size(&paths, &n, d);
+                if (r < 0)
+                        return r;
+        }
+
+        *ret = TAKE_PTR(paths);
+        return 0;
+}
+
 static int add_file_by_name(
                 sd_journal *j,
                 const char *prefix,