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After pursuing an MFA degree from New York University, Ali began his career as a regular on television series Crossing Jordan (2001–02) and Threat Matrix (2003–04), before his breakthrough role as Richard Tyler in the science fiction series The 4400 (2004–07). His first major film role was in the David Fincher-directed fantasy The Curious Case of Benjamin Button (2008). He gained wider attention for supporting roles in the final two films of the original The Hunger Games film series and in House of Cards, for which he received his first Primetime Emmy Award nomination.

Ali won the Academy Award for Best Supporting Actor for his performances as a drug dealer in the drama Moonlight (2016) and as Don Shirley in the comedy-drama Green Book (2018). He is the first Black actor to win two Academy Awards in the same category and the second Black actor to win multiple acting Oscars. Ali won the Primetime Emmy Award for Outstanding Children's Program for executive producing We Are the Dream: The Kids of the Oakland MLK Oratorical Fest (2020).

In 2019, he played a troubled police officer in the third season of the HBO anthology crime series True Detective, and in 2020, he starred in the second season of the Hulu comedy-drama series Ramy. He was nominated for Primetime Emmy Awards for both performances. Ali has also played Cornell "Cottonmouth" Stokes in the first season of the Netflix series Luke Cage (2016) and voiced Aaron Davis in the animated films Spider-Man: Into the Spider-Verse (2018) and Spider-Man: Across the Spider-Verse (2023).