diff --git a/src/run/run.c b/src/run/run.c
index 1f2938f9ea..5d2298a5f6 100644
--- a/src/run/run.c
+++ b/src/run/run.c
@@ -862,7 +862,8 @@ static int parse_argv_sudo_mode(int argc, char *argv[]) {
                         break;
 
                 case 'D':
-                        r = parse_path_argument(optarg, true, &arg_working_directory);
+                        /* Root will be manually suppressed later. */
+                        r = parse_path_argument(optarg, /* suppress_root= */ false, &arg_working_directory);
                         if (r < 0)
                                 return r;
 
@@ -901,6 +902,10 @@ static int parse_argv_sudo_mode(int argc, char *argv[]) {
                         if (r < 0)
                                 return log_error_errno(r, "Failed to get current working directory: %m");
                 }
+        } else {
+                /* Root was not suppressed earlier, to allow the above check to work properly. */
+                if (empty_or_root(arg_working_directory))
+                        arg_working_directory = mfree(arg_working_directory);
         }
 
         arg_service_type = "exec";
diff --git a/test/test-functions b/test/test-functions
index 269cd8812b..8a4cc55626 100644
--- a/test/test-functions
+++ b/test/test-functions
@@ -211,6 +211,7 @@ BASICTOOLS=(
     ping
     pkill
     ps
+    pwd
     readlink
     realpath
     rev
diff --git a/test/units/TEST-74-AUX-UTILS.run.sh b/test/units/TEST-74-AUX-UTILS.run.sh
index 9e0a429e41..5b46e11409 100755
--- a/test/units/TEST-74-AUX-UTILS.run.sh
+++ b/test/units/TEST-74-AUX-UTILS.run.sh
@@ -246,4 +246,16 @@ if [[ -e /usr/lib/pam.d/systemd-run0 ]] || [[ -e /etc/pam.d/systemd-run0 ]]; the
     # Let's chain a couple of run0 calls together, for fun
     readarray -t cmdline < <(printf "%.0srun0\n" {0..31})
     assert_eq "$("${cmdline[@]}" bash -c 'echo $SUDO_USER')" "$USER"
+
+    # Tests for working directory, especially for specifying "/" (see PR #34771).
+    cd /
+    assert_eq "$(run0 pwd)" "/"
+    assert_eq "$(run0 -D /tmp pwd)" "/tmp"
+    assert_eq "$(run0 --user=testuser pwd)" "/home/testuser"
+    assert_eq "$(run0 -D /tmp --user=testuser pwd)" "/tmp"
+    cd /tmp
+    assert_eq "$(run0 pwd)" "/tmp"
+    assert_eq "$(run0 -D / pwd)" "/"
+    assert_eq "$(run0 --user=testuser pwd)" "/home/testuser"
+    assert_eq "$(run0 -D / --user=testuser pwd)" "/"
 fi