Benjamin's comedy career began at age twenty-four in Boston where he was in a comedy duo with Sam Seder, then a member of Cross Comedy, a comedy team led by David Cross. For approximately the first seven years of his career, Benjamin almost exclusively worked in groups rather than independently. Afterwards, his independent work remained more experimental, rejecting traditional styles of stand-up comedy.
Benjamin's live projects include the Midnight Pajama Jam, a show performed in New York City with Jon Glaser, and Tinkle, a show combining stand-up comedy and live music co-hosted by Todd Barry and David Cross. A Midnight Pajama Jam DVD is currently in production. He and Cross also appear together on the album Invite Them Up.
He was the guest on Space Ghost Coast to Coast in its eighty-first episode "King Dead" on December 17, 1999 where Zorak and Moltar kidnapped him. He has appeared in the television show Cheap Seats, on ESPN Classic, as "Gene Stapleton" and "Rabbi Marc Shalowitz". He co-starred in Todd Barry's short film Borrowing Saffron, and portrayed a talking can of vegetables with a shameful habit of autofellatio in the film Wet Hot American Summer. He also made short cameos in Not Another Teen Movie as the football trainer and on the FX Network comedy-drama Rescue Me as the pimp "F-bomb" in season two. He can also be seen in Turbocharge- the Unauthorized Story of the Cars, a comedy biopic about 80's rock band The Cars, playing the role of Cars' manager Elliot Roberts in his usual deadpan comedic delivery.
Benjamin has done extensive voice work in animated TV shows. His credits include starring roles in several Soup2Nuts cartoon shows, such as Science Court, Home Movies, O'Grady, Dr. Katz, Professional Therapist, and Assy McGee. He also co-created the show Freak Show with his friend David Cross. Benjamin also starred as the Devil and multiple other roles in Lucy, the Daughter of the Devil, which ran for one season on Adult Swim beginning September 9, 2007. Benjamin also plays a recurring character on the PBS Kids series WordGirl, and is the announcer for The Sam Seder Show and the recently revived The Majority Report. He also did the voice of "Shelly", Sam Seder's accountant, on Breakroom Live with Maron & Seder.
Benjamin has made guest appearances in several animated shows. He was in the Aqua Teen Hunger Force episodes "Bus of the Undead" and "The Last One" as Mothmonsterman, in "Broodwich" as Mr. Sticks, in "Bible Fruit" as Mortimer Mango, and played the live-action role of Master Shake in "Last Last One Forever and Ever", credited as Capt. Turd Mahoy. He also made a cameo appearance as a government agent in the film Aqua Teen Hunger Force Colon Movie Film for Theaters alongside frequent collaborator Jon Glaser. He has appeared in Family Guy as Carl, a movie trivia obsessed convenience store clerk who also portrayed Yoda in the Star Wars parody episode "Something, Something, Something, Dark Side". Other notable recent appearances include The Venture Bros., in the episodes "Escape to the House of Mummies Part II," "I Know Why the Caged Bird Kills," and "The Better Man," in which he played Dr. Orpheus's master—who appears in the form of Cerberus, Catherine the Great's horse and, in "The Better Man", both Dr. Orpheus's ex-wife and a future Dean Venture, respectively. He also appeared in the Stella short "Bar", which can be found as an easter egg on the Season 1 DVD. Benjamin appeared on the Comedy Central sketch/variety show Important Things with Demetri Martin and had nearly as much screen time as Martin himself. In 2009 Benjamin, along with David Cross, created and wrote for Paid Programming, a live action television pilot for Cartoon Network's late night programing block, Adult Swim. Paid Programming was not picked up for a full series, this was confirmed when Benjamin referred to it as an "abject failure".
Benjamin was featured in a Super Bowl XLIII Bud Light commercial with Conan O'Brien and was responsible for the McCain Girls videos on YouTube. He voices Sterling Archer, a secret agent in the FX series Archer that first aired January 14, 2010. He has also appeared in several segments of the television show Human Giant and had a cameo in the American Dad! episode "License to Till" as a talking head of cabbage.
Benjamin starred in the Comedy Central series Jon Benjamin Has a Van, which he co-created with comedian Leo Allen. The series debuted on May 14, 2011; a total of 10 episodes aired, the last on August 10, 2011.
Beginning in 2013, Benjamin's voice can be heard as the narrator of a series of TV commercials for Coke Zero, including some with tie-ins to ESPN's College Game Day program.
In 2014 Benjamin was named as the year's best male comedy performer for his work on Bob's Burgers and Archer by the Vulture TV Awards, a digital expansion of New York magazine
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