Film and television work
He began by appearing in such television programmes as Lorna Doone, John Ridd and Evelyn Waugh's wartime saga Sword of Honour, and in Mike Leigh's film Topsy-Turvy. He played Mr Coxe in 1999's BBC version of Wives and Daughters. In 2000, Coyle's big break arrived, the character Jeff Murdock in the sitcom Coupling. In 2003 he chose not to return to Coupling for its fourth series, and refused requests to return for a "goodbye episode". In a 2005 interview, Coyle stated this was to avoid typecasting:
I'm very proud to have been part of Coupling and very grateful for the chance to play Jeff but I was very keen that that character didn’t stick with me forever. I’m an actor and I want to be an actor when I’m 60. It’s a lifelong process; why cut it off by boxing yourself into a little pigeonhole early on?
He also starred in the short-lived 2002–2003 BBC show Strange, and had roles in the films Human Traffic, Franklyn, and A Good Year. He appeared in the new special episode of Cracker: Nine Eleven in October 2006 (TV) and starred in The Whistleblowers on ITV. He also starred in the 2001 version of Othello as Michael Cassio.
In 2004, Coyle played the role of Alcock, body servant to John Wilmot, 2nd Earl of Rochester, in The Libertine alongside Johnny Depp. He appeared in Mike Newell's 2010 film Prince of Persia: The Sands of Time, playing Jake Gyllenhaal's older brother, the ambiguous Crown Prince Tus.
He was cast as the lead role, Moist von Lipwig, in the film Going Postal, based on the book of the same name by Terry Pratchett. This was broadcast on television in May 2010.
Coyle had a leading role in Renny Harlin's film 5 Days of War, about the 2008 war between Russia and Georgia over the territory of South Ossetia. In September 2011, Coyle appeared as William Winthrop, in Madonna's feature-directorial debut W.E. about the Duke and Duchess of Windsor. He appeared as Garda Ciarán O'Shea in Grabbers, the Irish comedy monster film. Coyle also plays Wallace in Outpost: Black Sun, the sequel to the 2008 British horror film Outpost, and the lead of drug pusher Frank in the 2012 English-language remake of Nicolas Winding Refn's 1996 cult classic Pusher.
In 2012, Coyle joined the cast of the USA Network show Covert Affairs as Simon Fischer, an FSB agent and love interest for Piper Perabo's Annie Walker. His character recurred until halfway through season three.
In 2014, NBC began airing the series Crossbones, with Coyle as Tom Lowe, who is assigned to kill the pirate Blackbeard (played by John Malkovich).
In 2018, Coyle was cast as Father Faustus Blackwood, a high priest of the Church of Night and Dean of the Academy of the Unseen Arts in the Netflix series Chilling Adventures of Sabrina.
In January 2021, Coyle announced via Instagram that he had been cast in Fantastic Beasts: The Secrets of Dumbledore, scheduled to be released in 2022 but said he could not disclose whom he was playing. When the trailer came out that December, it was confirmed that he would be playing Aberforth Dumbledore.
In 2026, in the BBC and BritBox adaptation of Janice Hadlow's Pride and Prejudice spinoff The Other Bennet Sister, Richard Coyle stars as Mr. Gardiner, alongside Indira Varma as Mrs Gardiner. He plays Mary Bennet's worldly and kind uncle who takes her under his wing, helping her gain confidence outside of her family's shadow.