In 2005, he appeared in a production of Prometheus Bound, which was revived in New York City in 2007. 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. He played the title role in Othello in 2016 at the New York Theatre Workshop with Daniel Craig as Iago, directed by Sam Gold.
Oyelowo is best known for playing MI5 officer Danny Hunter on the British drama series Spooks (known in North America as MI-5) from 2002 to 2004. He had before that appeared in Tomorrow La Scala (2002), Maisie Raine (1998) and Brothers and Sisters (1998); Soon after the end of his time on Spooks, Oyelowo made a cameo appearance in the Christmas special of As Time Goes By (2005). In 2006, he appeared in the television film Born Equal alongside Nikki Amuka-Bird as a couple fleeing persecution in Nigeria – they also both appeared in Shoot the Messenger (2006), and in The No. 1 Ladies’ Detective Agency (2008) as a husband and wife. Other cameos have included Mayo (guest-starring on 30 April 2006) and the television film Sweet Nothing in My Ear (2008, as defense attorney Leonard Grisham), while he has played recurring or main characters on 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. In March 2010, he played the role of Keme Tobodo in the BBC’s drama series Blood and Oil.
He starred in the HBO original film Nightingale (2014).
He appeared as Olaudah Equiano in Grace Unshackled – the Olaudah Equiano Story, a radio play adapting Equiano’s autobiography, The Interesting Narrative of the Life of Olaudah Equiano. This was first broadcast on BBC 7 on 8 April 2007, with his wife Jessica Oyelowo as Mrs. Equiano.
In 2007, Oyelowo was the reader for John le Carré’s The Mission Song. AudioFile magazine stated: “Think of David Oyelowo as a single musician playing all the instruments in a symphony.
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? This virtuoso performance makes that seem impossible.”] In 2015, he was selected to portray James Bond in Trigger Mortis, written by Anthony Horowitz.
As of 2014, he provides the voice of Imperial Security Bureau agent Alexandra Kallus on the animated series Star Wars Rebels.