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Akhtar is known for the bumbling Muslim extremist Faisal in Chris Morris's film Four Lions. Other comedic performances include Gupta in The Angelos Epithemiou Show, Maroush in The Dictator and Smee in Joe Wright and Pan.

Akhtar has also won acclaim for his dramatic performances: in 2015, he was nominated for a BAFTA for Best Supporting Actor for his 2014 role as Wilson Wilson on Channel 4's Utopia. He played shopkeeper Ahmed alongside Toby Jones in the BBC mini-series Capital, and DS Ira King in the BBC's River. Reviewing River in The Daily Telegraph, Michael Hogan wrote, "This series was beautifully written by Abi Morgan, stylishly directed, and most of all, superbly acted. The quieter, less showy supporting players also shone. Not just stalwarts [...] but fresher faces: Adeel Akhtar as River's endlessly patient sidekick and Georgina Rich as his psychiatrist".

In 2016 Akhtar appeared as Shahzad in the BBC one-off drama Murdered by My Father. He won the 2017 BAFTA award for Lead Actor for this role, the first non-white actor to do so. He also appeared as Rob Singhal in the acclaimed BBC miniseries based on John le Carré's The Night Manager.

Adeel became a patron of Half Moon Theatre in autumn 2016.