Miller grew up on a farm in Swoope, Virginia. After graduating from William & Mary, he moved to Knoxville, Tennessee in 1990. In 1994, he helped form a band called the Viceroys, which was renamed The V-Roys to avoid confusion with an existing group. The V-Roys were the first act signed on Steve Earle's label, E-Squared Records.
After the V-Roys split up in 1999, Miller formed a new band, Scott Miller and the Commonwealth, who were briefly the house band on Blue Collar TV. The Lexington Herald-Leader wrote of Miller's first albums after the V-Roys as "strong, folk-infused songs" in which "the boozy charm of his music was innocuous."
Miller's songs reflect his degrees in American history and Russian studies, with references to his home, family, history, geography, writers and Appalachia.
As of 2011, Miller was based in Staunton, Virginia, having moved back home to help manage the family cattle farm. Miller collaborated with filmmaker James Weems and photographer Glen Rose on mini-documentary Going Home which explores Miller's personal and musical journey in returning to the family farm.
As of 2015, in addition to solo shows, Miller played some shows with a full Commonwealth band lineup, but more often played trio shows with what he has come to call the Commonwealth Ladies Auxiliary (bass player Bryn Davies and fiddler Rayna Gellert).