diff --git a/airflow-core/src/airflow/settings.py b/airflow-core/src/airflow/settings.py
index 54150dd8bfd5b..148254f86c51c 100644
--- a/airflow-core/src/airflow/settings.py
+++ b/airflow-core/src/airflow/settings.py
@@ -241,13 +241,34 @@ def load_policy_plugins(pm: pluggy.PluginManager):
 
 
 def _get_async_conn_uri_from_sync(sync_uri):
-    # Mapping of backend to async driver:
+    """
+    Convert a sync SQLAlchemy URI to its async equivalent.
+
+    Args:
+        sync_uri: The synchronous SQLAlchemy connection URI
+
+    Returns:
+        The async URI with appropriate async driver (e.g., aiosqlite, asyncpg, aiomysql),
+        or the original URI if no async driver mapping exists
+
+    Raises:
+        ValueError: If the URI is malformed (missing ':' scheme separator)
+    """
+    # Mapping of backend to async driver.
     AIO_LIBS_MAPPING = {
         "sqlite": "aiosqlite",
         "postgresql": "psycopg_async" if _USE_PSYCOPG3 else "asyncpg",
         "mysql": "aiomysql",
     }
 
+    if not sync_uri or ":" not in sync_uri:
+        raise ValueError(
+            f"Invalid SQLAlchemy connection URI: {sync_uri!r}. "
+            "The URI must be in the format 'scheme://host/path' or similar with a ':' separator. "
+            "Check that AIRFLOW__DATABASE__SQL_ALCHEMY_CONN environment variable or "
+            "sql_alchemy_conn in airflow.cfg contains a valid database URI."
+        )
+
     scheme, rest = sync_uri.split(":", maxsplit=1)
     scheme = scheme.split("+", maxsplit=1)[0]
     aiolib = AIO_LIBS_MAPPING.get(scheme)
diff --git a/airflow-core/tests/unit/core/test_settings.py b/airflow-core/tests/unit/core/test_settings.py
index c703ee05ab941..7c0e48e825775 100644
--- a/airflow-core/tests/unit/core/test_settings.py
+++ b/airflow-core/tests/unit/core/test_settings.py
@@ -533,3 +533,62 @@ def test_early_return_when_all_none(self):
             settings.dispose_orm(do_log=False)
 
         mock_close.assert_not_called()
+
+
+class TestGetAsyncConnUriFromSync:
+    """Tests for _get_async_conn_uri_from_sync function."""
+
+    @pytest.mark.parametrize(
+        ("sync_uri", "expected"),
+        [
+            ("sqlite:///path/to/db.sqlite", "sqlite+aiosqlite:///path/to/db.sqlite"),
+            ("mysql://user:pass@localhost/dbname", "mysql+aiomysql://user:pass@localhost/dbname"),
+        ],
+    )
+    def test_supported_scheme_conversion(self, sync_uri, expected):
+        """Test conversion of supported sync SQLAlchemy URIs to async driver variants."""
+        result = settings._get_async_conn_uri_from_sync(sync_uri)
+        assert result == expected
+
+    @pytest.mark.parametrize(
+        ("sync_uri", "expected_template"),
+        [
+            ("postgresql://user:pass@localhost/dbname", "postgresql+{driver}://user:pass@localhost/dbname"),
+            ("postgresql+psycopg2://user@localhost/db", "postgresql+{driver}://user@localhost/db"),
+        ],
+    )
+    def test_postgresql_scheme_conversion(self, sync_uri, expected_template):
+        """Test conversion of PostgreSQL sync URIs to the configured async driver."""
+        postgres_async_driver = "psycopg_async" if settings._USE_PSYCOPG3 else "asyncpg"
+        assert settings._get_async_conn_uri_from_sync(sync_uri) == expected_template.format(
+            driver=postgres_async_driver
+        )
+
+    def test_unsupported_scheme_returns_original_uri(self):
+        """Test that unsupported schemes return the original URI unchanged."""
+        uri = "oracle://user:pass@localhost:1521/dbname"
+        result = settings._get_async_conn_uri_from_sync(uri)
+        assert result == uri
+
+    @pytest.mark.parametrize(
+        ("invalid_uri", "error_match"),
+        [
+            ("", "Invalid SQLAlchemy connection URI"),
+            (None, "Invalid SQLAlchemy connection URI"),
+            ("notavaliduri", "Invalid SQLAlchemy connection URI.*':' separator"),
+        ],
+    )
+    def test_invalid_uri_raises_value_error(self, invalid_uri, error_match):
+        """Test that invalid URIs raise ValueError with actionable guidance."""
+        with pytest.raises(ValueError, match=error_match):
+            settings._get_async_conn_uri_from_sync(invalid_uri)
+
+    def test_error_message_is_helpful(self):
+        """Test that error message contains helpful guidance."""
+        with pytest.raises(ValueError, match="Invalid SQLAlchemy connection URI") as exc_info:
+            settings._get_async_conn_uri_from_sync("invalid_value")
+
+        error_msg = str(exc_info.value)
+        assert "AIRFLOW__DATABASE__SQL_ALCHEMY_CONN" in error_msg
+        assert "sql_alchemy_conn" in error_msg
+        assert "airflow.cfg" in error_msg