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Cheadle's career started with supporting roles in Hamburger Hill (1987), Colors (1988), Devil in a Blue Dress (1995), Rosewood (1997), Boogie Nights (1997), and Bulworth (1998). He collaborated with director Steven Soderberghacting in Out of Sight (1998), Traffic (2000), The Ocean's Trilogy (2001–2007), and No Sudden Move (2021). Cheadle was nominated for an Academy Award for Best Actor for portraying Paul Rusesabagina in the historical drama film Hotel Rwanda (2004). He was the co-producer of Crash, which won the Academy Award for Best Picture in 2005. Cheadle joined the Marvel Cinematic Universe portraying James "Rhodey" Rhodes / War Machine, beginning with Iron Man 2 (2010).

On television, Cheadle earned nominations for the Primetime Emmy Award for Outstanding Lead Actor in a Comedy Series for his roles as Marty Kaan in House of Lies (2012–2016) and Maurice Monroe in Black Monday (2019–2021). He was further Emmy-nominated for The Rat Pack (1998), A Lesson Before Dying (1999), Things Behind the Sun (2001), ER (2002), and The Falcon and the Winter Soldier (2021).

In 2016, he received his first Grammy Award, winning Best Compilation Soundtrack for Visual Media for Miles Ahead's soundtrack. In 2022, he received a second Grammy for Best Spoken Word Album for his narration of the audiobook Carry On: Reflections for a New Generation from John Lewis; he also received a Tony Award for Best Musical as a producer for the musical A Strange Loop.