Brown received his bachelor's degree from Murray State University before moving to Chicago where he received his MFA from DePaul University Theatre School in 1989. After performing in numerous plays, including his breakout performance in Steppenwolf Theatre Company's outreach staging of Arthur Miller's A View from the Bridge, Brown began work in television and film. He appeared in such Chicago productions as Backdraft, The Babe, Excessive Force, Rookie of the Year and others.
In 1993, Brown moved to Los Angeles. He auditioned for, and was cast in Wes Craven's New Nightmare. He also has a minor role in Craven's Vampire in Brooklyn, and a bigger one as Gail's cameraman in Craven's Scream. Two years later, Brown played the role of Warren in the comedy film There's Something About Mary. Other past films credits include Being John Malkovich, Vanilla Sky, Dancing at the Blue Iguana, The Alamo, and The Big White. In 2009, Brown wrote and produced the Samuel Goldwyn Co./Sony release Bloodworth. Among Brown's more recent film credits are the Oscar-nominated films The Master and The Sessions and 2013's The Lone Ranger and Brother's Keeper, and 2014's Wild.
On television, Brown is best known for his portrayal of Dan Dority in HBO's Deadwood. During the show's second season, he was invited to join the show's writing staff by its creator, David Milch. In 2007, Brown earned a WGA nomination for writing on a drama series and a SAG nomination for best drama ensemble acting. Over the years, his numerous guest star roles on television include: Bates Motel, Rectify, Luck, American Horror Story, Justified, Six Feet Under, NYPD Blue, X-Files, The Mentalist, CSI: Crime Scene Investigation, Ellen, Seinfeld, True Detective, and others. Among the many TV movies he has been involved with was the starring role in VH1's Meatloaf: To Hell and Back.
In addition to his television and film work, Brown performed the motion capture and voiceover work for Naughty Dog's acclaimed video game, The Last of Us. He also writes and records with the Los Angeles band Sacred Cowboys, who performed around the Southwest U.S. steadily from 2005 to 2009, including having been on the bill for Stagecoach 2009, Southern California's premiere country music festival.