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Reilly started his career in the late 1980s, gaining recognition for his supporting roles in Casualties of War (1989), Days of Thunder (1990), Hard Eight(1996), Boogie Nights (1997), Magnolia (1999), Gangs of New York (2002) and The Aviator (2004). For his performance in the musical film Chicago (2002), he received nominations for the Academy Award and the Golden Globe Award for Best Supporting Actor.

Greater recognition came from Reilly's roles in comedy films Talladega Nights: The Ballad of Ricky Bobby (2006), Walk Hard: The Dewey Cox Story (2007), and Step Brothers (2008), in addition to his role as Dr. Steve Brule in the Adult Swimcomedy series Tim and Eric Awesome Show, Great Job! (2007–2010) and spinoff Check It Out! with Dr. Steve Brule (2010–2016). He provided the voice of the titular character in the Wreck-It Ralph films (2012–⁠2018). He starred in the independent films Cyrus (2010), We Need to Talk About Kevin and Carnage (both 2011), The Lobster (2015), The Sisters Brothers, and Stan & Ollie (both 2018). For his portrayal of comedian Oliver Hardy in the latter, he received critical acclaim and award nominations.

Reilly subsequently co-created and starred in the Showtime comedy series Moonbase 8 (2020) and the HBO sports drama series Winning Time: The Rise of the Lakers Dynasty (2022–2023). He also earned a nomination for the Children's and Family Emmy Award for his role in the Disney+ animated short film An Almost Christmas Story (2024). On stage, he received a nomination for the Tony Award for Best Actor in a Play for his role in the Broadway revival of Sam Shepard's play True West (2000). Aside from acting, Reilly also performs with his band John Reilly and Friends.