Cochrane's first roles included a part in a docudrama about drugs on Saturday Night with Connie Chung (1989) and an appearance in an episode of H.E.L.P. (1990). He then made his film debut (with about fifteen seconds' screen time) in A Kiss Before Dying, followed by his first substantial role as Jeff Goldblum's son in Fathers & Sons.
Cochrane played major roles in the films Empire Records and Dazed and Confused, with Jason London and Ben Affleck, and appeared in Hart's War starring Bruce Willis and Colin Farrell. He also appeared in the Richard Linklater film A Scanner Darkly (2006). Cochrane played the role of CSI Tim Speedle in CSI: Miami seasons 1-3. Cochrane reprised his role as Tim Speedle on CSI: Miami in the episode "Bang, Bang, Your Debt", as a hallucination to Detective Eric Delko in season 6.
In 2015, Cochrane had a supporting role as Boston mobster Stephen Flemmi in the true-crime film Black Mass, which starred Johnny Depp.
Featuring an excellent ensemble cast, a precise feel for the 1970s, and a killer soundtrack, Dazed and Confused is a funny, affectionate, and clear-eyed look at high school life.