diff --git a/.evergreen-functions.yml b/.evergreen-functions.yml
index daac22d9a5..3d9caeaeb7 100644
--- a/.evergreen-functions.yml
+++ b/.evergreen-functions.yml
@@ -50,6 +50,8 @@ variables:
       - VERSION_UPGRADE_HOOK_VERSION
       - BUILD_SCENARIO
       - MDB_BASH_DEBUG
+      - AI_MONGODB_EMBEDDING_INDEXING_KEY
+      - AI_MONGODB_EMBEDDING_QUERY_KEY
 
 functions:
 
@@ -584,6 +586,8 @@ functions:
           - github_pr_number
           - project_identifier
           - revision_order_id
+          - AI_MONGODB_EMBEDDING_INDEXING_KEY
+          - AI_MONGODB_EMBEDDING_QUERY_KEY
         add_to_path:
           - ${workdir}/bin
         binary: scripts/evergreen/e2e/e2e.sh
diff --git a/.evergreen-tasks.yml b/.evergreen-tasks.yml
index cae1ce3dab..fe9e0e2967 100644
--- a/.evergreen-tasks.yml
+++ b/.evergreen-tasks.yml
@@ -1323,6 +1323,11 @@ tasks:
     commands:
       - func: "e2e_test"
 
+  - name: e2e_search_community_auto_embedding
+    tags: ["patch-run"]
+    commands:
+      - func: "e2e_test"
+
   - name: e2e_search_community_tls
     tags: ["patch-run"]
     commands:
diff --git a/.evergreen.yml b/.evergreen.yml
index b0a44f065f..505e251e7c 100644
--- a/.evergreen.yml
+++ b/.evergreen.yml
@@ -663,6 +663,7 @@ task_groups:
     tasks:
       - e2e_community_replicaset_scale
       - e2e_search_community_basic
+      - e2e_search_community_auto_embedding
       - e2e_search_community_tls
       - e2e_search_external_basic
       - e2e_search_external_tls
diff --git a/docker/mongodb-kubernetes-tests/tests/common/search/movies_search_helper.py b/docker/mongodb-kubernetes-tests/tests/common/search/movies_search_helper.py
index be21511584..b639b3f6e7 100644
--- a/docker/mongodb-kubernetes-tests/tests/common/search/movies_search_helper.py
+++ b/docker/mongodb-kubernetes-tests/tests/common/search/movies_search_helper.py
@@ -27,6 +27,9 @@ def restore_sample_database(self):
     def create_search_index(self):
         self.search_tester.create_search_index(self.db_name, self.col_name)
 
+    def create_auto_embedding_vector_search_index(self):
+        self.search_tester.create_auto_embedding_vector_search_index(self.db_name, self.col_name)
+
     def wait_for_search_indexes(self):
         self.search_tester.wait_for_search_indexes_ready(self.db_name, self.col_name)
 
@@ -75,3 +78,51 @@ def execute_example_search_query(self):
                 {"$project": {"title": 1, "plot": 1, "genres": 1, "_id": 0}},
             ]
         )
+
+    def execute_auto_embedding_vector_search_query(self, query: str = "spy thriller", limit: int = 10):
+        return self.search_tester.client[self.db_name][self.col_name].aggregate(
+            [
+                {
+                    "$vectorSearch": {
+                        "index": "vector_auto_embed_index",
+                        "path": "plot",
+                        "query": query,
+                        "numCandidates": 150,
+                        "limit": limit,
+                    }
+                },
+                {
+                    "$project": {
+                        "_id": 0,
+                        "plot": 1,
+                        "title": 1,
+                        "score": {"$meta": "vectorSearchScore"},
+                    }
+                },
+            ]
+        )
+
+    def assert_auto_emb_vector_search_query(self, retry_timeout: int = 1):
+        def wait_for_auto_emb_search_results():
+            exp_document_count = 10
+            count = 0
+            status_msg = ""
+            try:
+                result = self.execute_auto_embedding_vector_search_query(limit=exp_document_count)
+                status_msg = f"{self.db_name}/{self.col_name}: auto-embedding vector search query results:\n"
+                for r in result:
+                    status_msg += f"{r}\n"
+                    count += 1
+                status_msg += f"Count: {count}"
+                logger.debug(status_msg)
+            except pymongo.errors.PyMongoError as e:
+                logger.debug(f"error: {e}")
+
+            return count == exp_document_count, status_msg
+
+        kubetester.run_periodically(
+            fn=wait_for_auto_emb_search_results,
+            timeout=retry_timeout,
+            sleep_time=1,
+            msg="Auto-embedding vector search query to return correct data",
+        )
diff --git a/docker/mongodb-kubernetes-tests/tests/common/search/search_tester.py b/docker/mongodb-kubernetes-tests/tests/common/search/search_tester.py
index 6dccfb5aeb..b32fa86264 100644
--- a/docker/mongodb-kubernetes-tests/tests/common/search/search_tester.py
+++ b/docker/mongodb-kubernetes-tests/tests/common/search/search_tester.py
@@ -45,6 +45,33 @@ def create_search_index(self, database_name: str, collection_name: str):
         result = collection.create_search_index(model=search_index_model)
         logger.debug(f"create_search_index result: {result}")
 
+    def create_auto_embedding_vector_search_index(
+        self,
+        database_name: str,
+        collection_name: str,
+        index_name: str = "vector_auto_embed_index",
+        field_path: str = "plot",
+        model: str = "voyage-4",
+    ):
+        database = self.client[database_name]
+        collection = database[collection_name]
+        search_index_model = SearchIndexModel(
+            definition={
+                "fields": [
+                    {
+                        "type": "autoEmbed",
+                        "modality": "text",
+                        "path": field_path,
+                        "model": model,
+                    }
+                ]
+            },
+            type="vectorSearch",
+            name=index_name,
+        )
+        result = collection.create_search_index(model=search_index_model)
+        logger.debug(f"create_auto_embedding_vector_search_index result: {result}")
+
     def wait_for_search_indexes_ready(self, database_name: str, collection_name: str, timeout=60):
         kubetester.run_periodically(
             fn=lambda: self.search_indexes_ready(database_name, collection_name),
diff --git a/docker/mongodb-kubernetes-tests/tests/search/search_community_auto_embedding.py b/docker/mongodb-kubernetes-tests/tests/search/search_community_auto_embedding.py
new file mode 100644
index 0000000000..3cad36cbac
--- /dev/null
+++ b/docker/mongodb-kubernetes-tests/tests/search/search_community_auto_embedding.py
@@ -0,0 +1,133 @@
+import os
+
+from kubetester import create_or_update_secret, try_load
+from kubetester.kubetester import fixture as yaml_fixture
+from kubetester.mongodb_community import MongoDBCommunity
+from kubetester.mongodb_search import MongoDBSearch
+from kubetester.phase import Phase
+from pytest import fixture, mark
+from tests import test_logger
+from tests.common.search import movies_search_helper
+from tests.common.search.movies_search_helper import SampleMoviesSearchHelper
+from tests.common.search.search_tester import SearchTester
+from tests.conftest import get_default_operator
+
+logger = test_logger.get_test_logger(__name__)
+
+ADMIN_USER_NAME = "mdb-admin-user"
+ADMIN_USER_PASSWORD = "mdb-admin-user-pass"
+
+MONGOT_USER_NAME = "search-sync-source"
+MONGOT_USER_PASSWORD = "search-sync-source-user-password"
+
+USER_NAME = "mdb-user"
+USER_PASSWORD = "mdb-user-pass"
+
+MDBC_RESOURCE_NAME = "mdbc-rs"
+EMBEDDING_INDEXING_KEY_ENV_VAR = "AI_MONGODB_EMBEDDING_INDEXING_KEY"
+EMBEDDING_QUERY_KEY_ENV_VAR = "AI_MONGODB_EMBEDDING_QUERY_KEY"
+VOYAGE_API_KEY_SECRET_NAME = "voyage-api-keys"
+PROVIDER_ENDPOINT = "https://ai.mongodb.com/v1/embeddings"
+
+
+@fixture(scope="function")
+def mdbc(namespace: str) -> MongoDBCommunity:
+    resource = MongoDBCommunity.from_yaml(
+        yaml_fixture("community-replicaset-sample-mflix.yaml"),
+        name=MDBC_RESOURCE_NAME,
+        namespace=namespace,
+    )
+
+    if try_load(resource):
+        return resource
+
+    return resource
+
+
+@fixture(scope="function")
+def mdbs(namespace: str) -> MongoDBSearch:
+    resource = MongoDBSearch.from_yaml(
+        yaml_fixture("search-minimal.yaml"),
+        namespace=namespace,
+    )
+
+    if try_load(resource):
+        return resource
+
+    return resource
+
+
+@mark.e2e_search_community_auto_embedding
+def test_install_operator(namespace: str, operator_installation_config: dict[str, str]):
+    operator = get_default_operator(namespace, operator_installation_config=operator_installation_config)
+    operator.assert_is_running()
+
+
+@mark.e2e_search_community_auto_embedding
+def test_install_secrets(namespace: str, mdbs: MongoDBSearch):
+    create_or_update_secret(namespace=namespace, name=f"{USER_NAME}-password", data={"password": USER_PASSWORD})
+    create_or_update_secret(
+        namespace=namespace, name=f"{ADMIN_USER_NAME}-password", data={"password": ADMIN_USER_PASSWORD}
+    )
+    create_or_update_secret(
+        namespace=namespace, name=f"{mdbs.name}-{MONGOT_USER_NAME}-password", data={"password": MONGOT_USER_PASSWORD}
+    )
+
+    indexing_key = os.getenv(EMBEDDING_INDEXING_KEY_ENV_VAR)
+    query_key = os.getenv(EMBEDDING_QUERY_KEY_ENV_VAR)
+    if not indexing_key or not query_key:
+        raise ValueError(
+            f"Missing required environment variables: {EMBEDDING_INDEXING_KEY_ENV_VAR} and/or {EMBEDDING_QUERY_KEY_ENV_VAR}"
+        )
+    create_or_update_secret(
+        namespace=namespace,
+        name=VOYAGE_API_KEY_SECRET_NAME,
+        data={"query-key": query_key, "indexing-key": indexing_key},
+    )
+
+
+@mark.e2e_search_community_auto_embedding
+def test_create_database_resource(mdbc: MongoDBCommunity):
+    mdbc.update()
+    mdbc.assert_reaches_phase(Phase.Running, timeout=300)
+
+
+@mark.e2e_search_community_auto_embedding
+def test_create_search_resource(mdbs: MongoDBSearch):
+    mdbs["spec"]["autoEmbedding"] = {
+        "embeddingModelAPIKeySecret": {"name": VOYAGE_API_KEY_SECRET_NAME},
+        "providerEndpoint": PROVIDER_ENDPOINT,
+    }
+    mdbs.update()
+    mdbs.assert_reaches_phase(Phase.Running, timeout=300)
+
+
+@mark.e2e_search_community_auto_embedding
+def test_wait_for_community_resource_ready(mdbc: MongoDBCommunity):
+    mdbc.assert_reaches_phase(Phase.Running, timeout=300)
+
+
+@fixture(scope="function")
+def sample_movies_helper(mdbc: MongoDBCommunity) -> SampleMoviesSearchHelper:
+    return movies_search_helper.SampleMoviesSearchHelper(
+        SearchTester(get_connection_string(mdbc, USER_NAME, USER_PASSWORD))
+    )
+
+
+@mark.e2e_search_community_auto_embedding
+def test_search_restore_sample_database(sample_movies_helper: SampleMoviesSearchHelper):
+    sample_movies_helper.restore_sample_database()
+
+
+@mark.e2e_search_community_auto_embedding
+def test_search_create_search_index(sample_movies_helper: SampleMoviesSearchHelper):
+    sample_movies_helper.create_auto_embedding_vector_search_index()
+
+
+@mark.e2e_search_community_auto_embedding
+def test_search_assert_search_query(sample_movies_helper: SampleMoviesSearchHelper):
+    sample_movies_helper.assert_auto_emb_vector_search_query(retry_timeout=90)
+
+
+def get_connection_string(mdbc: MongoDBCommunity, user_name: str, user_password: str) -> str:
+    return f"mongodb://{user_name}:{user_password}@{mdbc.name}-0.{mdbc.name}-svc.{mdbc.namespace}.svc.cluster.local:27017/?replicaSet={mdbc.name}"
diff --git a/scripts/evergreen/deployments/test-app/templates/mongodb-enterprise-tests.yaml b/scripts/evergreen/deployments/test-app/templates/mongodb-enterprise-tests.yaml
index 78194ae510..5a484b361d 100644
--- a/scripts/evergreen/deployments/test-app/templates/mongodb-enterprise-tests.yaml
+++ b/scripts/evergreen/deployments/test-app/templates/mongodb-enterprise-tests.yaml
@@ -198,6 +198,10 @@ spec:
       value: "{{ .Values.cognito_workload_url }}"
     - name: cognito_workload_user_id
       value: "{{ .Values.cognito_workload_user_id }}"
+    - name: AI_MONGODB_EMBEDDING_INDEXING_KEY
+      value: "{{ .Values.autoEmbedding.providerMongoDB.indexingKey }}"
+    - name: AI_MONGODB_EMBEDDING_QUERY_KEY
+      value: "{{ .Values.autoEmbedding.providerMongoDB.queryKey }}"
     image: "{{ .Values.mekoTestsRegistry }}/mongodb-kubernetes-tests:{{ .Values.mekoTestsVersion }}"
     # Options to pytest command should go in the pytest.ini file.
     command: ["pytest"]
diff --git a/scripts/evergreen/deployments/test-app/values.yaml b/scripts/evergreen/deployments/test-app/values.yaml
index 440dc56d43..6ada16e0e7 100644
--- a/scripts/evergreen/deployments/test-app/values.yaml
+++ b/scripts/evergreen/deployments/test-app/values.yaml
@@ -51,3 +51,8 @@ helm:
     registry: ""
     repository: ""
     region: ""
+
+autoEmbedding:
+  providerMongoDB:
+    indexingKey: ""
+    queryKey: ""
diff --git a/scripts/evergreen/e2e/single_e2e.sh b/scripts/evergreen/e2e/single_e2e.sh
index b43cb9205b..cfd845524b 100755
--- a/scripts/evergreen/e2e/single_e2e.sh
+++ b/scripts/evergreen/e2e/single_e2e.sh
@@ -89,6 +89,8 @@ deploy_test_app() {
         "--set" "helm.oci.registry=${helm_oci_registry}"
         "--set" "helm.oci.repository=${helm_oci_repository}"
         "--set" "helm.oci.region=${helm_oci_registry_region}"
+        "--set" "autoEmbedding.providerMongoDB.indexingKey=${AI_MONGODB_EMBEDDING_INDEXING_KEY}"
+        "--set" "autoEmbedding.providerMongoDB.queryKey=${AI_MONGODB_EMBEDDING_QUERY_KEY}"
     )
 
     # shellcheck disable=SC2154