The New Group later changed their name to The State. After performing their material at various theaters, bars and clubs in New York City, they started work on the MTV show You Wrote It, You Watch It. This led to the self-titled series The State (199395), which was nominated for a Cable Ace Award for Best Comedy Series.

Following the collapse of The State after a one-night stint on CBS, Lennon, along with Kenney, Ben Garant, and Michael Ian Black went on to create and star in the Comedy Central program Viva Variety (199799). The show was based on a sketch that Lennon had written for the final season of The State, called "The Mr. and Former Mrs. Laupin Variety Programme". Viva Variety received a Cable Ace Award nomination for Best Comedy Series. After Viva Variety, Lennon, Kenney and Garant created and starred in another TV show, Reno 911! (200309). Initially slated for FOX, the program later debuted on Comedy Central. The show is currently syndicated around the world.

Lennon has appeared in dozens of TV shows, including The League, Children's Hospital, Archer, New Girl, Comedy Bang Bang, Don't Trust the B---- in Apartment 23, and is a cult favorite as Joey Tribbiani's blackjack dealing, "identical hand twin" on the Friends fifth season finale ("The One In Vegas," Pts. I and II). He has also appeared in supporting roles in dozens of films, including Bad Teacher, Memento, How To Lose A Guy In 10 Days and I Love You, Man, for which he and costar Paul Rudd were nominated for an MTV Movie Award for Best Kiss. He has appeared on Jimmy Kimmel Live!, The Tonight Show, The Daily Show, Late Night with Jimmy Fallon, Talkshow with Spike Feresten, and he holds a record, for his number of appearances on The Late Late Show with Craig Ferguson, both as himself and as Lt. Dangle.

Lennon appeared as a doctor in the Christopher Nolan films Memento (2000) and The Dark Knight Rises (2012). Lennon has done various voice work, including the shows Kim Possible, Bob's Burgers, and Planet Sheen, in which he played the character of Pinter.

He plays the "The Reading Fairie" in the Tinkerbell movie: Tinkerbell and the Secret of the Wings. He played the voice of Eddie the Shipboard computer in the film version of The Hitchhiker's Guide to the Galaxy.

Lennon has also written for comic books. For The Goon, he wrote a short story called "Jimmy Turtle and the Legendary Box Car of Well-Made Ladies Shoes" and another for Dwight T. Albatross's The Goon Noir #3. He also wrote "The Pigmy Elixir" for Bart Simpson's Treehouse of Horror #13.

He is frequently a presenter at the Eisner Awards, given out each year at Comic-Con.

In 2008, Lennon started doing stand-up comedy, during which he will sometimes play guitar. He appears frequently at Comedy Death Ray in Los Angeles, and he was the photo for the month of July in the Comedy Death Ray 2010 Calendar.

In 2009, he opened for Stella (starring The State and Viva Variety! alumni Michael Ian Black, Michael Showalter and David Wain) at the Orpheum Theatre in Los Angeles. Also in 2009, The State reunited at the Eureka Theatre for two shows at San Francisco's Sketchfest, performing all new material.

The shows sold out in minutes.

Lennon and Garant created and starred in a 2010 sitcom pilot for NBC called The Strip. However, in May 2010 it was announced that NBC had decided not to produce it as a series.

Lennon filled in as guest voice for the robot sidekick Geoff Peterson on the CBS show The Late Late Show with Craig Ferguson in November and December 2011.

In 2012 he guest starred as Neil in the final episode of season one of New Girl.

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