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He voiced the title character in the commercially successful animated film Wreck-It Ralph (2012), and appeared in the superhero film Guardians of the Galaxy (2014), as well as Kong: Skull Island (2017).Since 2010, Reilly has been starring in the television series Check It Out! Steve Brule, playing the titular character that originated on Tim and Eric Awesome Show, Great Job! Reilly performs with his band John Reilly and Friends and worked as a stage actor in True West (2000), for which he was nominated for the Tony Award for Best Actor in a Play.Reilly collaborated with filmmaker Paul Thomas Anderson in his directorial debut Hard Eight (1996), playing a man in need of ,000 to pay for the burial of his mother, who is taken under the wing of experienced gambler Sydney (Philip Baker Hall).

In 2002, he played the role of Amos Hart, Roxie Hart's naïve husband, in the musical film Chicago.In 2006, he performed two songs on Rogue's Gallery: Pirate Ballads, Sea Songs, and Chanteys: "Fathom the Bowl" and "My Son John".Reilly gained exposure through his supporting roles in Days of Thunder (1990), What's Eating Gilbert Grape (1993), and The River Wild (1994).He also starred in Paul Thomas Anderson's films, Hard Eight (1996), Boogie Nights (1997) and Magnolia (1999).In Chicago, he played Amos Hart, Roxanne's (Renée Zellweger) trusting husband and was nominated for the Academy Award for Best Supporting Actor, as well as the Golden Globe for Best Supporting Actor.

Martin Scorsese's Gangs of New York featured Reilly as corrupt 19th-century constable "Happy Jack" Mulraney, while Stephen Daldry's drama The Hours saw him play the husband to Julianne Moore's character.

In 2011, he recorded songs produced by Jack White and released as two singles by White's Third Man Records.

The first single features two The Delmore Brothers songs: "Gonna Lay Down My Old Guitar" and "Lonesome Yodel Blues #2", both performed with Tom Brosseau.

Reilly may be one of our finer character actors, but his portrayal of Richard Gaddis, a gimlet-eyed con man, in Criminal allows too many vestiges of the duped schlub of a husband he played in Chicago to leak into his performance." Reilly co-starred in Adam Mc Kay's comedy about NASCAR drivers entitled Talladega Nights: The Ballad of Ricky Bobby in August 2006 as Cal Naughton Jr., the best friend and teammate of the title character, played by Will Ferrell. Steve Brule, which has aired since 2010 and is written and produced by Reilly.

Reilly frequently appeared on the sketch comedy program Tim and Eric Awesome Show, Great Job! In early 2011, Reilly collaborated with director Miguel Arteta for a second time with the comedy Cedar Rapids, starring Ed Helms.

His character in the film was Franklin, the father of the troubled Kevin; His last release of 2011 was Roman Polanski's black comedy-drama Carnage, which takes place mostly in a single apartment.