Bentley is best known for his roles as Ricky Fitts in American Beauty (1999), Blackheart in Ghost Rider (2007), Thomas in P2 (2007), Seneca Crane in The Hunger Games (2012), and Doyle in Interstellar (2014). He was one of four subjects in the documentary My Big Break (2009), which covered his fame after American Beauty and struggles with substance abuse. Rebuilding his career, he starred in the premiere of Venus in Fur by David Ives in the off-Broadway production in 2010.
He began appearing in the FX anthology series American Horror Story in 2014, playing Edward Mordrake in Freak Show. In 2015, he starred as Detective John Lowe in Hotel, for which he received a Critics' Choice Television Award nomination. The following year, he played Ambrose White in the series' sixth cycle, subtitled Roanoke.