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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.
In 2014, Miller became engaged to his longtime girlfriend, actress and installation artist Kate Gorney, who changed her last name to Miller. They were married at the Denver Botanic Gardens on September 6, 2015
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 is worldwide known for playing the charater Weasel in the Deadpool films, based upon the Marvel Comics character Deadpool. He also starred in the Fox TV series 'The Goodwin Games' as Jimmy Goodwin. Miller also appeared 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 around him in 2017, and he was replaced by comedian Jason Mantzoukas. In 2017 and 2018 different allegations of Sexual assault, sending transphobic emails and work misconduct were all made againt Miller.
Miller was arrested on the night of April 9, 2018, at LaGuardia Airport in Queens, New York on federal charges related to a fake bomb threat made while aboard an Amtrak train. On April 10, 2018, he was released on a $100,000 bond following an appearance at a federal court hearing in New Haven, Connecticut. If convicted, he could face up to five years in prison. In September 2018, it was reported that Miller was negotiating a plea deal to avoid a trial. As a result of this and the sexual assault allegations, DreamWorks Animation removed Miller from How to Train Your Dragon: The Hidden World, with Justin Rupple overdubbing his lines as Tuffnut.
- According to Alex Hirsch, when Miller first saw the character design for Dipper, his initial reaction was "Pfft, looks like a dork."