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Holmes has appeared on Comedy Central's Premium Blend, as a regular panelist on VH1's Best Week Ever, and on VH1's All Access.[3] His cartoonshave appeared in The New Yorker.[4] In 2010, he performed on John Oliver's New York Stand Up Show as well as Late Night with Jimmy Fallon. On February 26, 2010, he performed his first television special on the series Comedy Central Presents. On March 21, 2011 and on November 17, 2011, he appeared on the TBS talk show Conan.

Holmes has provided the voices for several of the characters on Comedy Central's cartoon Ugly Americans. He was the voice of the E-Trade baby on several television commercials and was also credited as a writer for those commercials.

He wrote for the NBC primetime sitcom Outsourced and also wrote for the Fox sitcom I Hate My Teenage Daughter prior to its cancellation in May 2012.

Holmes released his first album, Impregnated With Wonder, on iTunes on November 15, 2011. It was named one of the best comedy CDs of 2011 byThe A.V. Club.[5] In 2013, he released his second album, Nice Try, The Devil, which was also named as one of the best comedy CDs of 2013 by the Onion A.V. Club.

Holmes is also known for his comedic portrayal of Batman in CollegeHumor's internet series Badman. The series recreates scenes from Christopher Nolan's Batman films with a comedic twist, such as Batman appearing completely incompetent or sex-obsessed.