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Miller was born in Denver, Colorado. He attended Graland Country Day School, East High School and George Washington University in Washington, D.C. where he was a member of the comedy group GWU recess and the Lambda chapter of Phi Sigma Kappa.
Miller appears frequently as a member of the "round table" on Chelsea Lately. He appeared as Marmaduke Brooker in the TV series Carpoolers which ran for 13 episodes on ABC in 2007-2008. On December 13, 2010, October 28, 2011, and June 14, 2012, he performed stand-up on Conan. On November 15, 2011, T. J. Miller's stand-up special "No Real Reason" premiered on Comedy Central. In 2011, he hosted a special called Mash Up, which was picked up in 2012 for a full season by Comedy Central and premiered to rave reviews. Miller starred in Fox TV series The Goodwin Games as Jimmy Goodwin. Miller currently appears in Mike Judge's series Silicon Valley on HBO, and was the voice of a talking ball of mucus in commercials for Mucinex, until sexual assault allegations arose, and he was replaced by comedian Jason Mantzoukas.
- According to Alex Hirsch, when Miller first saw the character design for Dipper, his initial reaction was "Pfft, looks like a dork."