The Vermont National Guard includes four O-6 level commands: the Army National Guard's 86th Infantry Brigade Combat Team (Mountain), 124th Regional Training School, and Garrison Support Command, as well as the Air National Guard's 158th Fighter Wing. It also includes Joint Force Headquarters, which includes command structure and staff agencies. 

The Vermont National Guard has a dual mission that consists of both federal and state roles. For state missions, the governor, through the state adjutant general, commands Guard forces. The governor can call the National Guard into action during local or statewide emergencies, such as storms, fires, pandemic response, or civil disturbances.

In addition, the president of the United States can activate the National Guard for participation in federal missions. Examples of federal activations include Guard units deployed to Europe and Africa for stabilization operations and units deployed to the Middle East and other locations in the War on Terrorism. When federalized, Guard units are commanded by the combatant commander of the theatre in which they are operating.