diff --git a/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/RestVectorTileAction.java b/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/RestVectorTileAction.java
index 442f0176444bd..f14333c8f6328 100644
--- a/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/RestVectorTileAction.java
+++ b/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/RestVectorTileAction.java
@@ -11,6 +11,7 @@
 
 import org.elasticsearch.action.search.SearchRequestBuilder;
 import org.elasticsearch.action.search.SearchResponse;
+import org.elasticsearch.action.support.IndicesOptions;
 import org.elasticsearch.client.internal.node.NodeClient;
 import org.elasticsearch.common.document.DocumentField;
 import org.elasticsearch.common.geo.GeoBoundingBox;
@@ -45,6 +46,7 @@
 import org.elasticsearch.search.aggregations.metrics.InternalGeoBounds;
 import org.elasticsearch.search.aggregations.pipeline.StatsBucketPipelineAggregationBuilder;
 import org.elasticsearch.search.aggregations.support.ValuesSourceAggregationBuilder.MetricsAggregationBuilder;
+import org.elasticsearch.search.crossproject.CrossProjectModeDecider;
 import org.elasticsearch.search.fetch.subphase.FieldAndFormat;
 import org.elasticsearch.search.profile.SearchProfileResults;
 import org.elasticsearch.search.sort.SortBuilder;
@@ -91,10 +93,12 @@ public class RestVectorTileAction extends BaseRestHandler {
 
     private final SearchUsageHolder searchUsageHolder;
     private final Settings settings;
+    private final CrossProjectModeDecider crossProjectModeDecider;
 
     public RestVectorTileAction(SearchUsageHolder searchUsageHolder, Settings settings) {
         this.searchUsageHolder = searchUsageHolder;
         this.settings = settings;
+        this.crossProjectModeDecider = new CrossProjectModeDecider(settings);
     }
 
     @Override
@@ -109,15 +113,23 @@ public String getName() {
 
     @Override
     protected RestChannelConsumer prepareRequest(RestRequest restRequest, NodeClient client) throws IOException {
-        if (settings != null && settings.getAsBoolean("serverless.cross_project.enabled", false)) {
-            // accept but drop project_routing param until fully supported
-            restRequest.param("project_routing");
-        }
+        boolean crossProjectEnabled = crossProjectModeDecider.crossProjectEnabled();
 
         // This will allow to cancel the search request if the http channel is closed
         final RestCancellableNodeClient cancellableNodeClient = new RestCancellableNodeClient(client, restRequest.getHttpChannel());
         final VectorTileRequest request = VectorTileRequest.parseRestRequest(restRequest, searchUsageHolder::updateUsage);
         final SearchRequestBuilder searchRequestBuilder = searchRequestBuilder(cancellableNodeClient, request);
+
+        if (crossProjectEnabled && request.allowsCrossProject()) {
+            searchRequestBuilder.setIndicesOptions(
+                IndicesOptions.builder(searchRequestBuilder.request().indicesOptions())
+                    .crossProjectModeOptions(new IndicesOptions.CrossProjectModeOptions(true))
+                    .build()
+            );
+        } else if (crossProjectEnabled == false && request.getProjectRouting() != null) {
+            throw new IllegalArgumentException("Unknown key for a VALUE_STRING in [project_routing]");
+        }
+
         return channel -> searchRequestBuilder.execute(new RestResponseListener<>(channel) {
 
             @Override
@@ -288,10 +300,10 @@ private static SearchRequestBuilder searchRequestBuilder(RestCancellableNodeClie
         for (SortBuilder<?> sortBuilder : request.getSortBuilders()) {
             searchRequestBuilder.addSort(sortBuilder);
         }
+        searchRequestBuilder.request().setProjectRouting(request.getProjectRouting());
         return searchRequestBuilder;
     }
 
-    @SuppressWarnings("unchecked")
     private static VectorTile.Tile.Layer.Builder buildHitsLayer(SearchHit[] hits, VectorTileRequest request, FeatureFactory featureFactory)
         throws IOException {
         final VectorTile.Tile.Layer.Builder hitsLayerBuilder = VectorTileUtils.createLayerBuilder(HITS_LAYER, request.getExtent());
diff --git a/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/VectorTileRequest.java b/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/VectorTileRequest.java
index 69f44d64d6b6d..2638e172c913f 100644
--- a/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/VectorTileRequest.java
+++ b/x-pack/plugin/vector-tile/src/main/java/org/elasticsearch/xpack/vectortile/rest/VectorTileRequest.java
@@ -7,9 +7,11 @@
 
 package org.elasticsearch.xpack.vectortile.rest;
 
+import org.elasticsearch.action.IndicesRequest;
 import org.elasticsearch.common.Strings;
 import org.elasticsearch.common.geo.SimpleVectorTileFormatter;
 import org.elasticsearch.core.Booleans;
+import org.elasticsearch.core.Nullable;
 import org.elasticsearch.geometry.Rectangle;
 import org.elasticsearch.index.query.AbstractQueryBuilder;
 import org.elasticsearch.index.query.GeoShapeQueryBuilder;
@@ -46,7 +48,7 @@
 /**
  * Transforms a rest request in a vector tile request
  */
-class VectorTileRequest {
+class VectorTileRequest implements IndicesRequest.CrossProjectCandidate {
 
     protected static final String INDEX_PARAM = "index";
     protected static final String FIELD_PARAM = "field";
@@ -61,6 +63,7 @@ class VectorTileRequest {
     protected static final ParseField BUFFER_FIELD = new ParseField("buffer");
     protected static final ParseField EXACT_BOUNDS_FIELD = new ParseField("exact_bounds");
     protected static final ParseField WITH_LABELS_FIELD = new ParseField("with_labels");
+    protected static final ParseField PROJECT_ROUTING = new ParseField("project_routing");
 
     protected static class Defaults {
         public static final int SIZE = 10000;
@@ -131,6 +134,7 @@ protected static class Defaults {
                 return p.intValue();
             }
         }, SearchSourceBuilder.TRACK_TOTAL_HITS_FIELD, ObjectParser.ValueType.VALUE);
+        PARSER.declareString(VectorTileRequest::setProjectRouting, PROJECT_ROUTING);
     }
 
     static VectorTileRequest parseRestRequest(RestRequest restRequest, Consumer<SearchUsage> searchUsageConsumer) throws IOException {
@@ -221,6 +225,9 @@ static VectorTileRequest parseRestRequest(RestRequest restRequest, Consumer<Sear
     private boolean with_labels = Defaults.WITH_LABELS;
     private int trackTotalHitsUpTo = Defaults.TRACK_TOTAL_HITS_UP_TO;
 
+    @Nullable
+    private String projectRouting;
+
     private VectorTileRequest(String[] indexes, String field, int z, int x, int y) {
         this.indexes = indexes;
         this.field = field;
@@ -322,6 +329,24 @@ public int getGridPrecision() {
         return gridPrecision;
     }
 
+    @Override
+    public boolean allowsCrossProject() {
+        return true;
+    }
+
+    public void setProjectRouting(String projectRouting) {
+        if (this.projectRouting != null) {
+            throw new IllegalArgumentException("project_routing is already set to [" + this.projectRouting + "]");
+        }
+
+        this.projectRouting = projectRouting;
+    }
+
+    @Nullable
+    public String getProjectRouting() {
+        return this.projectRouting;
+    }
+
     private void setGridPrecision(int gridPrecision) {
         if (gridPrecision < 0) {
             throw new IllegalArgumentException("[gridPrecision] parameter cannot be negative, found [" + gridPrecision + "]");