diff --git a/src/resolve/resolved-link-bus.c b/src/resolve/resolved-link-bus.c
index a269414ccf..0f341d740a 100644
--- a/src/resolve/resolved-link-bus.c
+++ b/src/resolve/resolved-link-bus.c
@@ -392,6 +392,10 @@ int bus_link_method_set_domains(sd_bus_message *message, void *userdata, sd_bus_
                         dns_search_domain_move_back_and_unmark(d);
                 else {
                         r = dns_search_domain_new(l->manager, &d, DNS_SEARCH_DOMAIN_LINK, l, /* delegate= */ NULL, name);
+                        if (r == -E2BIG) {
+                                changed = dns_search_domain_unlink_marked(l->search_domains) || changed;
+                                r = dns_search_domain_new(l->manager, &d, DNS_SEARCH_DOMAIN_LINK, l, /* delegate= */ NULL, name);
+                        }
                         if (r < 0)
                                 goto clear;
 
diff --git a/test/units/TEST-75-RESOLVED.sh b/test/units/TEST-75-RESOLVED.sh
index ad4e8f8a42..44cc71ba9f 100755
--- a/test/units/TEST-75-RESOLVED.sh
+++ b/test/units/TEST-75-RESOLVED.sh
@@ -290,6 +290,21 @@ manual_testcase_01_resolvectl() {
     assert_in "DOMAINS=~route-only-change.example.com" "$(cat "$hoge_state")"
     assert_not_in "route-only-change.example.com" "$(cat /run/systemd/resolve/resolv.conf /run/systemd/resolve/stub-resolv.conf)"
 
+    resolvectl domain hoge "old.example.com"
+    local domains=()
+    for i in {1..1025}; do
+        domains+=("too-many-$i.example.com")
+    done
+    (! resolvectl domain hoge "${domains[@]}")
+    assert_in 'old.example.com' "$(resolvectl domain hoge)"
+
+    domains=()
+    for i in {1..1024}; do
+        domains+=("replacement-$i.example.com")
+    done
+    resolvectl domain hoge "${domains[@]}"
+    assert_not_in 'old.example.com' "$(resolvectl domain hoge)"
+    assert_in 'replacement-1024.example.com' "$(resolvectl domain hoge)"
     echo -e "nameserver 10.0.2.1\ndomain test-domain.example.com" | SYSTEMD_INVOKED_AS=resolvconf resolvectl -x -a hoge
     assert_in 'test-domain.example.com' "$(resolvectl domain hoge)"
     assert_in '~.' "$(resolvectl domain hoge)"