diff --git a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/AbstractRemoteClusterSecurityTestCase.java b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/AbstractRemoteClusterSecurityTestCase.java
index 2c61707f57a5a..52ae569df1230 100644
--- a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/AbstractRemoteClusterSecurityTestCase.java
+++ b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/AbstractRemoteClusterSecurityTestCase.java
@@ -7,6 +7,8 @@
 
 package org.elasticsearch.xpack.remotecluster;
 
+import io.netty.handler.codec.http.HttpMethod;
+
 import org.apache.http.HttpHost;
 import org.apache.http.client.methods.HttpPost;
 import org.elasticsearch.client.Request;
@@ -25,6 +27,7 @@
 import org.elasticsearch.test.cluster.util.resource.Resource;
 import org.elasticsearch.test.rest.ESRestTestCase;
 import org.elasticsearch.test.rest.ObjectPath;
+import org.elasticsearch.xpack.security.SecurityFeatures;
 import org.junit.AfterClass;
 import org.junit.BeforeClass;
 
@@ -33,8 +36,11 @@
 import java.nio.charset.StandardCharsets;
 import java.util.Arrays;
 import java.util.Base64;
+import java.util.List;
 import java.util.Locale;
 import java.util.Map;
+import java.util.Set;
+import java.util.stream.Collectors;
 
 import static org.hamcrest.Matchers.anEmptyMap;
 import static org.hamcrest.Matchers.equalTo;
@@ -78,6 +84,7 @@ public abstract class AbstractRemoteClusterSecurityTestCase extends ESRestTestCa
         .configFile("remote-cluster-client.key", Resource.fromClasspath("ssl/remote-cluster-client.key"))
         .configFile("remote-cluster-client.crt", Resource.fromClasspath("ssl/remote-cluster-client.crt"))
         .configFile("remote-cluster-client-ca.crt", Resource.fromClasspath("ssl/remote-cluster-client-ca.crt"))
+        .configFile("signing.crt", Resource.fromClasspath("signing/signing.crt"))
         .module("reindex") // Needed for the role metadata migration
         .user(USER, PASS.toString());
 
@@ -197,8 +204,10 @@ protected void configureRemoteCluster(
         boolean isProxyMode,
         boolean skipUnavailable
     ) throws Exception {
+        putFulfillingClusterSettings();
+
         // For configurable remote cluster security, this method assumes the cross cluster access API key is already configured in keystore
-        putRemoteClusterSettings(clusterAlias, targetFulfillingCluster, basicSecurity, isProxyMode, skipUnavailable);
+        putQueryClusterSettings(clusterAlias, targetFulfillingCluster, basicSecurity, isProxyMode, skipUnavailable);
 
         // Ensure remote cluster is connected
         checkRemoteConnection(clusterAlias, targetFulfillingCluster, basicSecurity, isProxyMode);
@@ -234,7 +243,18 @@ protected void reloadSecureSettings() throws IOException {
         }
     }
 
-    protected void putRemoteClusterSettings(
+    protected void putFulfillingClusterSettings() throws IOException {
+        if (getFulfillingClusterNodeFeatures().contains(SecurityFeatures.CERTIFICATE_IDENTITY_FIELD_FEATURE.id())) {
+            final var request = newXContentRequest(HttpMethod.PUT, "/_cluster/settings", (builder, params) -> {
+                builder.startObject("persistent");
+                Settings.builder().put("cluster.remote.signing.certificate_authorities", "signing.crt").build().toXContent(builder, params);
+                return builder.endObject();
+            });
+            assertOK(performRequestAgainstFulfillingCluster(request));
+        }
+    }
+
+    protected void putQueryClusterSettings(
         String clusterAlias,
         ElasticsearchCluster targetFulfillingCluster,
         boolean basicSecurity,
@@ -303,6 +323,22 @@ protected static String randomEncodedApiKey() {
             .encodeToString((UUIDs.base64UUID() + ":" + UUIDs.randomBase64UUIDSecureString()).getBytes(StandardCharsets.UTF_8));
     }
 
+    protected Set<String> getFulfillingClusterNodeFeatures() throws IOException {
+        final Request request = new Request("GET", "_cluster/state");
+        request.addParameter("filter_path", "nodes_features");
+        final Response response = performRequestAgainstFulfillingCluster(request);
+
+        var responseData = responseAsMap(response);
+        if (responseData.get("nodes_features") instanceof List<?> nodesFeatures) {
+            return nodesFeatures.stream().map(Map.class::cast).flatMap(nodeFeatureMap -> {
+                @SuppressWarnings("unchecked")
+                List<String> features = (List<String>) nodeFeatureMap.get("features");
+                return features.stream();
+            }).collect(Collectors.toSet());
+        }
+        return Set.of();
+    }
+
     protected record TestClusterConfigProviders(LocalClusterConfigProvider server, LocalClusterConfigProvider client) {}
 
     protected static TestClusterConfigProviders EMPTY_CONFIG_PROVIDERS = new TestClusterConfigProviders(cluster -> {}, cluster -> {});
diff --git a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityBWCToRCS2ClusterRestIT.java b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityBWCToRCS2ClusterRestIT.java
index c62a18602ae2d..05d0218b65292 100644
--- a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityBWCToRCS2ClusterRestIT.java
+++ b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityBWCToRCS2ClusterRestIT.java
@@ -40,8 +40,6 @@ public class RemoteClusterSecurityBWCToRCS2ClusterRestIT extends AbstractRemoteC
             .setting("xpack.ml.enabled", "false")
             .setting("remote_cluster_server.enabled", "true")
             .setting("remote_cluster.port", "0")
-            .setting("cluster.remote.signing.certificate_authorities", "signing.crt")
-            .configFile("signing.crt", Resource.fromClasspath("signing/signing.crt"))
             .setting("xpack.security.remote_cluster_server.ssl.enabled", "true")
             .setting("xpack.security.remote_cluster_server.ssl.key", "remote-cluster.key")
             .setting("xpack.security.remote_cluster_server.ssl.certificate", "remote-cluster.crt")
diff --git a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityReloadCredentialsRestIT.java b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityReloadCredentialsRestIT.java
index fb941e9e815cf..8eb19e435bb45 100644
--- a/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityReloadCredentialsRestIT.java
+++ b/x-pack/plugin/security/qa/multi-cluster/src/javaRestTest/java/org/elasticsearch/xpack/remotecluster/RemoteClusterSecurityReloadCredentialsRestIT.java
@@ -197,7 +197,7 @@ private void configureRcs2() throws Exception {
         final boolean configureSettingsFirst = randomBoolean();
         // it's valid to first configure remote cluster, then credentials
         if (configureSettingsFirst) {
-            putRemoteClusterSettings("my_remote_cluster", fulfillingCluster, false, isProxyMode, randomBoolean());
+            putQueryClusterSettings("my_remote_cluster", fulfillingCluster, false, isProxyMode, randomBoolean());
         }
 
         configureRemoteClusterCredentials("my_remote_cluster", remoteClusterCredentials, keystoreSettings);