diff --git a/airflow-core/src/airflow/config_templates/config.yml b/airflow-core/src/airflow/config_templates/config.yml
index b3bc911e1d859..cbec251ada8f0 100644
--- a/airflow-core/src/airflow/config_templates/config.yml
+++ b/airflow-core/src/airflow/config_templates/config.yml
@@ -509,6 +509,19 @@ core:
       type: string
       example: ~
       default: ~
+    template_searchpath:
+      description: |
+        Path where Airflow looks for Jinja templates used in DAGs and task fields.
+        Can be a single absolute path (string) or a comma-separated list of multiple
+        absolute paths.
+        When multiple paths are specified, Airflow searches them in the provided order
+        until the requested template file is found. Relative paths are resolved against
+        ``AIRFLOW_HOME``.
+      version_added: 3.1.0
+      type: string
+      example: "/opt/airflow/dags/templates,/opt/airflow/cutom_templates"
+      default: ~
+
 database:
   description: ~
   options:
diff --git a/airflow-core/tests/unit/models/test_dag.py b/airflow-core/tests/unit/models/test_dag.py
index 53cafab354334..21f962c059144 100644
--- a/airflow-core/tests/unit/models/test_dag.py
+++ b/airflow-core/tests/unit/models/test_dag.py
@@ -323,6 +323,66 @@ def test_resolve_template_files_list(self, tmp_path):
 
         assert task.test_field == ["{{ ds }}", "some_string"]
 
+    def test_template_searchpath_from_config(self, tmp_path, monkeypatch):
+        # Create a template file
+        template_dir = tmp_path
+        path = template_dir / "searchpath_testfile.template"
+        path.write_text("{{ ds }}")
+
+        # Patch config to include tmp_path as template_searchpath
+        monkeypatch.setenv("AIRFLOW__CORE__TEMPLATE_SEARCHPATH", str(tmp_path))
+
+        with DAG(
+            dag_id="test-dag",
+            schedule=None,
+            start_date=DEFAULT_DATE,
+        ):
+            task = EmptyOperator(task_id="op1")
+
+        task.test_field = path.name  # only the file name, not full path
+        task.template_fields = ("test_field",)
+        task.template_ext = (".template",)
+        task.resolve_template_files()
+
+        assert task.test_field == "{{ ds }}"
+
+    def test_listof_template_searchpath_from_config(self, tmp_path, monkeypatch):
+        # create two template files in two different directories
+        dir1 = tmp_path / "templates1"
+        dir2 = tmp_path / "templates2"
+        dir1.mkdir()
+        dir2.mkdir()
+
+        template_file1 = dir1 / "file1.txt"
+        template_file2 = dir2 / "file2.txt"
+        template_file1.write_text("Hello from template1")
+        template_file2.write_text("{{ ds }}")
+
+        # Case 1: multiple paths (list of strings)
+
+        monkeypatch.setenv("AIRFLOW__CORE__TEMPLATE_SEARCHPATH", f"{str(dir1)},{str(dir2)}")
+        with DAG(
+            dag_id="test-dag-multi",
+            schedule=None,
+            start_date=DEFAULT_DATE,
+        ):
+            task1 = EmptyOperator(task_id="op1")
+            task2 = EmptyOperator(task_id="op2")
+
+            # Test task1 loads template from dir1
+            task1.test_field = "file1.txt"
+            task1.template_fields = ("test_field",)
+            task1.template_ext = (".txt",)
+            task1.resolve_template_files()
+            assert "Hello" in task1.test_field
+
+            # Test task2 loads template from dir2
+            task2.test_field = "file2.txt"
+            task2.template_fields = ("test_field",)
+            task2.template_ext = (".txt",)
+            task2.resolve_template_files()
+            assert "{{ ds }}" in task2.test_field
+
     def test_create_dagrun_when_schedule_is_none_and_empty_start_date(self, testing_dag_bundle):
         # Check that we don't get an AttributeError 'start_date' for self.start_date when schedule is none
         dag = DAG("dag_with_none_schedule_and_empty_start_date", schedule=None)
diff --git a/task-sdk/src/airflow/sdk/definitions/dag.py b/task-sdk/src/airflow/sdk/definitions/dag.py
index 7448b321389cb..23e7953dafff3 100644
--- a/task-sdk/src/airflow/sdk/definitions/dag.py
+++ b/task-sdk/src/airflow/sdk/definitions/dag.py
@@ -737,13 +737,21 @@ def resolve_template_files(self):
 
     def get_template_env(self, *, force_sandboxed: bool = False) -> jinja2.Environment:
         """Build a Jinja2 environment."""
+        from airflow.configuration import conf
         from airflow.sdk.definitions._internal.templater import NativeEnvironment, SandboxedEnvironment
 
         # Collect directories to search for template files
         searchpath = [self.folder]
+
+        # First priority: template_searchpath passed by user
         if self.template_searchpath:
             searchpath += self.template_searchpath
 
+        # Always include config path as a fallback source
+        # Developers don't need to configure template_searchpath in every DAG — they can rely on a global value from airflow.cfg
+        if config_path := conf.get("core", "template_searchpath", fallback=""):
+            searchpath.extend(p.strip() for p in config_path.split(","))
+
         # Default values (for backward compatibility)
         jinja_env_options = {
             "loader": jinja2.FileSystemLoader(searchpath),