diff --git a/server/src/main/java/org/opensearch/cluster/metadata/MetadataIndexTemplateService.java b/server/src/main/java/org/opensearch/cluster/metadata/MetadataIndexTemplateService.java
index a7b9eba6dbc05..a2e69fefef87c 100644
--- a/server/src/main/java/org/opensearch/cluster/metadata/MetadataIndexTemplateService.java
+++ b/server/src/main/java/org/opensearch/cluster/metadata/MetadataIndexTemplateService.java
@@ -52,6 +52,7 @@
 import org.opensearch.common.Priority;
 import org.opensearch.common.UUIDs;
 import org.opensearch.common.ValidationException;
+import org.opensearch.common.collect.Tuple;
 import org.opensearch.common.compress.CompressedXContent;
 import org.opensearch.common.inject.Inject;
 import org.opensearch.common.logging.HeaderWarning;
@@ -474,6 +475,29 @@ static void validateNotInUse(Metadata metadata, String templateNameOrWildcard) {
                     + templatesStillUsing
             );
         }
+
+        validateNoIndexUsesContext(metadata, matchingComponentTemplates);
+    }
+
+    /**
+     * Validate that a system template is not being used directly by an index.
+     */
+    static void validateNoIndexUsesContext(Metadata metadata, Set<String> matchingComponentTemplates) {
+        List<Tuple<String, String>> indicesUsingSpecifiedContexts = metadata.indices()
+            .values()
+            .stream()
+            .filter(imd -> imd.context() != null)
+            .filter(imd -> matchingComponentTemplates.contains(findContextTemplateName(metadata, imd.context())))
+            .map(imd -> Tuple.tuple(imd.getIndex().getName(), findContextTemplateName(metadata, imd.context())))
+            .collect(Collectors.toList());
+
+        if (!indicesUsingSpecifiedContexts.isEmpty()) {
+            throw new IllegalArgumentException(
+                "Cannot process request to remove component templates as they are being used by indices."
+                    + "First few indices preventing the deletion are: "
+                    + indicesUsingSpecifiedContexts.subList(0, Math.min(10, indicesUsingSpecifiedContexts.size()))
+            );
+        }
     }
 
     /**
diff --git a/server/src/test/java/org/opensearch/cluster/metadata/MetadataIndexTemplateServiceTests.java b/server/src/test/java/org/opensearch/cluster/metadata/MetadataIndexTemplateServiceTests.java
index 8312267205d62..d310eda69e76c 100644
--- a/server/src/test/java/org/opensearch/cluster/metadata/MetadataIndexTemplateServiceTests.java
+++ b/server/src/test/java/org/opensearch/cluster/metadata/MetadataIndexTemplateServiceTests.java
@@ -81,6 +81,8 @@
 import java.util.Map;
 import java.util.Objects;
 import java.util.Set;
+import java.util.TreeMap;
+import java.util.UUID;
 import java.util.concurrent.CountDownLatch;
 import java.util.concurrent.TimeUnit;
 import java.util.concurrent.atomic.AtomicReference;
@@ -2017,6 +2019,43 @@ public void testRemoveComponentTemplateInUse() throws Exception {
         );
     }
 
+    public void testValidateNoIndexUsesContextWithIndexUsingContext() throws Exception {
+        String contextName = "testcontext";
+        String indexName = "index";
+        Metadata metadata = mock(Metadata.class);
+        when(metadata.systemTemplatesLookup()).thenReturn(Map.of(contextName, new TreeMap<>() {
+            {
+                put(1L, contextName);
+            }
+        }));
+
+        IndexMetadata indexMetadata = mock(IndexMetadata.class);
+        when(indexMetadata.context()).thenReturn(new Context(contextName));
+        when(indexMetadata.getIndex()).thenReturn(new Index(indexName, UUID.randomUUID().toString()));
+        when(metadata.indices()).thenReturn(Map.of(indexName, indexMetadata));
+
+        expectThrows(
+            IllegalArgumentException.class,
+            () -> MetadataIndexTemplateService.validateNoIndexUsesContext(metadata, Set.of(contextName))
+        );
+    }
+
+    public void testValidateNoIndexUsesContextWithNoIndexUsingContext() throws Exception {
+        String contextName = "testcontext";
+        String indexName = "index";
+        Metadata metadata = mock(Metadata.class);
+        when(metadata.systemTemplatesLookup()).thenReturn(Map.of(contextName, new TreeMap<>() {
+            {
+                put(1L, contextName);
+            }
+        }));
+
+        IndexMetadata indexMetadata = mock(IndexMetadata.class);
+        when(metadata.indices()).thenReturn(Map.of(indexName, indexMetadata));
+
+        MetadataIndexTemplateService.validateNoIndexUsesContext(metadata, Set.of(contextName));
+    }
+
     /**
      * Tests that we check that settings/mappings/etc are valid even after template composition,
      * when adding/updating a composable index template