In film, Dillahunt has played supporting roles in No Country for Old Men, The Assassination of Jesse James by the Coward Robert Ford, Winter's Bone, Looper, and 12 Years a Slave.

Garret Dillahunt was born in Castro Valley, California, the middle of three boys, and was raised in Selah, Washington, a suburb of Yakima.

He appeared as a regular in several short lived series on ABC and Showtime, and landed guest spots on TV shows such as The X-Files and NYPD Blue[6] among others, before playing two distinctly different characters on the HBO series Deadwood: Jack McCall in 2004 and Francis Wolcott in 2005 (Dillahunt returned in an uncredited role as a townsman in the 2019 Deadwood movie).

Later roles included Dr. Michael Smith on HBO's John from Cincinnati; Cromartie, John Henry and George Laszlo on FOX's Terminator: The Sarah Connor Chronicles; Roman Nevikov, a Russian gangster, on NBC's Life; and Mason Turner, a paralyzed serial killer on Criminal Minds.

He played Simon Escher in the Burn Notice third-season finale airing March 4, 2010 on USA, later reprising the role in the show's fourth and seventh seasons.