diff --git a/lib/spack/spack/config.py b/lib/spack/spack/config.py
index 1cafc1f738a..50d7caa5c3d 100644
--- a/lib/spack/spack/config.py
+++ b/lib/spack/spack/config.py
@@ -672,11 +672,12 @@ def set(self, path: str, value: Any, scope: Optional[str] = None) -> None:
             return
 
         parts = process_config_path(path)
-        section = parts.pop(0)
+        section = parts[0]
 
         section_data = self.get_config(section, scope=scope)
 
-        data = section_data
+        full_data = {section: section_data}
+        data = full_data
         while len(parts) > 1:
             key = parts.pop(0)
 
@@ -699,7 +700,7 @@ def set(self, path: str, value: Any, scope: Optional[str] = None) -> None:
         # update new value
         data[parts[0]] = value
 
-        self.update_config(section, section_data, scope=scope)
+        self.update_config(section, full_data[section], scope=scope)
 
     def __iter__(self):
         """Iterate over scopes in this configuration."""
diff --git a/lib/spack/spack/test/config.py b/lib/spack/spack/test/config.py
index 52e1cc9e04a..50e2e1b7588 100644
--- a/lib/spack/spack/test/config.py
+++ b/lib/spack/spack/test/config.py
@@ -1208,8 +1208,16 @@ def test_internal_config_list_override(mock_low_high_config, write_config_file):
 def test_set_section_override(mock_low_high_config, write_config_file):
     write_config_file("config", config_merge_list, "low")
     wanted_list = config_override_list["config"]["build_stage:"]
+
+    # Ensure test validity:
+    assert wanted_list != mock_low_high_config.get("config:build_stage")
+
+    # Test both bare section with full value and section override in path
     with spack.config.override("config::build_stage", wanted_list):
         assert mock_low_high_config.get("config:build_stage") == wanted_list
+    with spack.config.override("config::", {"build_stage": wanted_list}):
+        assert mock_low_high_config.get("config:build_stage") == wanted_list
+
     assert config_merge_list["config"]["build_stage"] == mock_low_high_config.get(
         "config:build_stage"
     )