He also achieved praise for his roles as Louis Gaines in The Butler (2013), Seretse Khama in A United Kingdom (2016) and Robert Katende in Queen of Katwe (2016).

He has also played supporting roles in the films Rise of the Planet of the Apes (2011), The Help (2011), Lincoln (2012), Red Tails (2012), and Jack Reacher (2012).

On television, Oyelowo has played MI5 officer Danny Hunter in the British drama series Spooks (2002–2004) and Javert in the BBC miniseries Les Misérables (2018).

[8] Oyelowo is an omoba (or prince) of the Yoruba people in the Nigerian chieftaincy system, his grandfather having been king of "a part of Oyo State called Awe".

[14] He began his stage career in 1999 when he was offered a season with the Royal Shakespeare Company playing roles in Ben Jonson's Volpone, as the title character in Oroonoko (which he also performed in the BBC radio adaptation) and Shakespeare's Antony and Cleopatra (1999) alongside Guy Henry, Frances de la Tour and Alan Bates.

In a major landmark for colour-blind casting, Oyelowo was the first black actor to play an English king in a major production of Shakespeare, and although this casting choice was initially criticised by some in the media, Oyelowo's performance was critically acclaimed and later won the 2001 Ian Charleson Award for best performance by an actor under 30 in a classical play.

In 2006, he made his directorial debut on a production of The White Devil, produced by Inservice, his theatre company in Brighton which is co-run with fellow Brighton-based actors Priyanga Burford, Israel Aduramo, Penelope Cobbuld, and his wife, Jessica.

[15] He played the title role in Othello in 2016 at the New York Theatre Workshop with Daniel Craig as Iago, directed by Sam Gold.

Other cameos have included Mayo (guest-starring on 30 April 2006) and the television film Sweet Nothing in My Ear (2008, as defence attorney Leonard Grisham), while he has played recurring or main characters in Five Days (2007) and The Passion (2008, as Joseph of Arimathea).

In December 2009, he played the leading role of Gilbert in the BBC TV adaptation of Andrea Levy's novel Small Island.

That is essentially what he manages in this inspired performance of John le Carré's suspense novel.... Can it really have been only one man in the narrator's recording booth?

[21] As of 2014[update], he provides the voice of Imperial Security Bureau agent Alexsandr Kallus on the animated series Star Wars Rebels.

That same year Oyelowo appeared in Lee Daniels' The Paperboy, which competed for the Palme d'Or at the 2012 Cannes Film Festival.

He was slated to star with Lupita Nyong'o in a film adaptation of the Chimamanda Ngozi Adichie novel Americanah but scheduling conflicts meant the project never moved forward.

In February 2019, it was announced that Oyelowo had joined the Peter Rabbit cast with James Corden, Rose Byrne and Domhnall Gleeson reprising their roles as the title character, Bea and Thomas McGregor for its sequel due to be released in March 2021.

[32] For his portrayal of Martin Luther King Jr. in Selma, Oyelowo received the NAACP Image Award for Outstanding Actor in a Motion Picture.