Mapother was born in Louisville, Kentucky, the son of Louisa (née Riehm) and William Reibert Mapother Sr (c.1938–2006). His father was an attorney, bankruptcy consultant, and judge in Louisville between 1967 and 1970. William Sr. died on June 22, 2006 as a result of lung cancer and pulmonary fibrosis. Mapother Jr. is a first cousin of actor Tom Cruise, whose birth name is Thomas Cruise Mapother IV.
Mapother has become widely known as a character actor, and sometimes plays scary or otherwise dark characters. He played a pivotal role in Todd Field's In the Bedroom, and is perhaps best known as Ethan Rom in the TV show Lost, which he played for 11 episodes during the life of the series.
Mapother has also had considerable roles in a series of independent films, such as The Lather Effect, Moola, Hurt, and Another Earth. Mapother starred in The Burrowers as a Native American fighter who joins a posse to help find missing white settlers.

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