Dunne began his professional acting career at age 19 with a small supporting role in The Other Side of the Mountain in 1975. He has since appeared on both film and television, starring in An American Werewolf in London (1981) as Jack Goodman, Johnny Dangerously (1984) as Tommy Kelly, After Hours (1985) as Paul Hackett, Who's That Girl (1987) as Loudon Trott opposite Madonna, My Girl (1991) as Jake Bixler, Quiz Show (1994) as the Geritol Account Executive, Game 6 (2005) as Elliott Litvak and I Like It Like That (1994) as Stephen Price. Dunne also played Dr. Vass, opposite Matthew McConaughey, in the Oscar-nominated 2013 film Dallas Buyers Club.
Dunne was born Thomas Griffin Dunne in New York City, the son of Ellen Beatriz (née Griffin) and Dominick Dunne. He is the older brother of Alexander and Dominique Dunne. His mother founded the victims' rights organization Justice for Homicide Victims after Dominique's murder in 1982. His father was a Producer, Writer, and actor. He is also the nephew of John Gregory Dunne and Joan Didion. Raised in Los Angeles, Dunne attended the Fay School in Southborough, Massachusetts and then went to high school in Colorado Springs, Colorado where he developed an interest in acting, appearing in many school plays. He was scheduled to perform in a school production of Othello when on the eve of a performance, Dunne was found smoking marijuana by a Teacher. He was immediately expelled and soon after, he moved back to New York to pursue his acting interests.
Dunne's directorial debut was the 1995 short film Duke of Groove. Since then, he has directed five feature films, including Addicted to Love (1997) and Practical Magic (1998). He also directed one segment of the 2012 anthology film Movie 43. Dunne produced and directed Joan Didion: The Center Will Not Hold (2017), a documentary about his aunt, author Joan Didion, whom Dunne interviews and appears with on screen.
In July 2009, he married his second wife, Anna Bingemann, an Australian Stylist.
Dunne's TV appearances include Frasier, Saturday Night Live, Alias, and Law & Order: Criminal Intent (Episodes 5, 118, and 128). He portrayed Tony Mink in the comedy Trust Me on TNT. In 2012, Dunne guest-starred as management consultant Marco Pelios in seven episodes of the premiere season of the Showtime TV series House of Lies.
