Oakes began his career at
Shakespeare's Globe, before taking roles at the
Almeida Theatre and the
Old Vic. Since appearing at
Shakespeare's Globe at the outset of his career, Oakes has frequently performed in numerous rehearsed readings as part of their "
Read Not Dead" initiative, including their landmark 200th reading of
Philip Massinger's
A New Way To Pay Old Debts; Oakes played Wellborn alongside a cast including
Benjamin Whitrow,
Alan Cox, and
Nicholas Rowe. In 2006, Oakes performed a 90-minute abridged version of
Much Ado About Nothing as part of the
Royal Shakespeare Company's "Complete Works" festival along with his final year graduates from the Bristol Old Vic Theatre School. He alternated between playing Claudio and Verges alongside fellow graduate
Matt Barber. ,
Hofburg Imperial Palace, Vienna, 2011 Oakes was present to accept the Jury Prize at the 2011
Romy Awards in
Vienna alongside
Donald Sutherland and
Natalia Wörner. Oakes came to prominence when he played the villainous William Hamleigh in the television
miniseries The Pillars of the Earth (2010). The following year, Oakes was cast in the television series
The Borgias (2011), airing on
Showtime. Whilst shooting the second season, Oakes performed a cameo in the sequel to
The Pillars of the Earth,
World Without End (2012). Between 2010 and 2013, Oakes had several roles playing villains on television—such as William Hamleigh in
The Pillars of the Earth (2010),
Juan Borgia in
The Borgias (2011), and
George, Duke of Clarence in
The White Queen (2013). When he played
Mr. Darcy in an adaptation of
Pride and Prejudice at
Open Air Theatre, Regent's Park in 2013, he said, "I've been playing bad guys back to back, so Darcy's a bit of an antidote!" Arostus,
John Lyly's ''
Love's Metamorphosis'' as Montanus, and
Thomas Middleton's
Your Five Gallants as Tailby. In a return to TV period dramas in 2015, Oakes guest-starred in both the third season of
Endeavour with
Shaun Evans and in
BBC's limited series
The Living and the Dead with
Colin Morgan. He played
Prince Ernest, brother of
Queen Victoria's husband
Prince Albert, in the 2016 ITV series
Victoria. The role reunited Oakes with his
Trinity co-star
Tom Hughes, and
Pillars of the Earth co-star
Rufus Sewell. In 2017, Oakes starred in the film adaptation of
Albert Sánchez Piñol's novel
Cold Skin, directed by
Xavier Gens and co-starring
Ray Stevenson and
Aura Garrido. He also starred as Thomas Novachek in the London West End premiere of
David Ives's play
Venus in Fur at the
Theatre Royal Haymarket. This production was directed by
Patrick Marber and co-starred
Natalie Dormer as Vanda. Oakes played
Earl Godwin in
Vikings: Valhalla, the spin-off of the show
Vikings, for
Netflix. Oakes set up a theatre company called Dog Ate Cake with a long-term theatrical collaborator Henry Bell. In 2015 Oakes starred as Banquo in a charity fundraiser for the
Shakespeare Schools Festival. The event was largely improvised by the actors and lawyers involved, but based on a framework written by
Jonathan Myerson. The cast also included
Christopher Eccleston as Macbeth,
Haydn Gwynne as Lady Macbeth,
Paterson Joseph as MacDuff, and
Pippa Bennett-Warner as one of the Weird Sisters. The event interrupted the events of the original play following the death of Duncan, placing Macbeth on trial for murder. Oakes, Joseph, and Gwynne appeared as witnesses for the prosecution while Eccleston and Bennett-Warner played witnesses for the defence. The event was overseen by High Court Judge
Sir Michael Burton; the QCs were John Kelsey-Fry,
Jonathan Laidlaw,
Dinah Rose, and
Ian Winter, and the foreman of the jury was
Jeremy Paxman. In 2019, Oakes played
Hamlet at Shakespeare's Rose Theatre,
York.
The Stage wrote that he "plays Hamlet with natural ease: he is clearly comfortable with the cadences of the language and he conveys meaning well." Both
WhatsOnStage and the
British Theatre Guide praised Oakes' performance, particularly his rapport with the audience, despite the production's more light-hearted take on the play. In 2025, Oakes starred in a production of “
Anna Karenina” at
Chichester Festival Theatre. He appeared as “Kostya” Levin in the parallel storyline to that of his real-world partner,
Natalie Dormer, who played the role of Anna. Oakes’ performance garnered universal praise.
The Times said, “Oakes wins our sympathy as Levin”, whilst
The Guardian stated that: “…the relationship that sparks most on stage is that between Levin (based on Tolstoy himself, played by David Oakes) and Kitty, from its humour to its tenderness.”
Whatsonstage praised his performance as being "wonderfully still".
Theatre direction Oakes has directed a number of theatre pieces alongside his acting career. In 2003 he took a stage adaptation of
The Wicker Man to the Epping Forest Theatre Festival. Rehearsing in and around his hometown of Salisbury, Oakes "got kicked out of the [Cathedral] Close for rehearsing pagan rituals for [his] open-air production of
The Wicker Man." While at university, Oakes directed numerous plays including
Martin McDonagh's
Beauty Queen of Leenane,
Harold Pinter's
The Dumb Waiter and
Anthony Minghella's
Whale Music. Also whilst at University in 2005, Oakes assisted director Natalie Wilson on a production of ''Smilin' Through'' that was co-produced by the Truant Company,
Birmingham Repertory Theatre, and
Contact Theatre,
Manchester. Later that year, Oakes once again turned to literary adaptation, taking a production of
Stephen King's
The Boogeyman to the
Edinburgh Festival Fringe. Oakes frequently directs at Shakespeare's Globe extending their "Read Not Dead" series, a study devoted to performing fully staged readings of the entirety of the
Early Modern Canon of Drama. Most recently Oakes directed
Robert Greene's
The Honourable History of Friar Bacon and Friar Bungay and
Lewis Theobald's "Happy Ending" version of
John Webster's
The Duchess of Malfi, "The Fatal Secret". Oakes recently directed an extract of
Robert Daborne's ''
A Christian Turn'd Turk'' as part of a special "Read Not Dead" event at Shakespeare's Globe. Four directors with four scholars were teamed up with actors and presented their arguments and selected scenes at a special hustings event on Thursday 29 May 2014. Winning the event, teamed with Dr Emma Smith of Oxford University, Oakes directed the full play on Sunday 5 October 2014 in the Sam Wanamaker Playhouse.
Podcasts In 2020, Oakes narrated an episode of
Historic Royal Palaces'
Outliers podcast. He appeared as
Thomas Phelippes, a spy and code breaker in the court of
Elizabeth I plotting the downfall of
Mary, Queen of Scots. Oakes is the presenter of the natural history podcast
Trees A Crowd. The first episode was released on 25 February 2019 and featured Mark Frith. ==Personal life==