Riley's television credits include episodes of Poirot (2003), Marple (2006), Doctor Who (2008's "Silence in the Library" and "Forest of the Dead"). She played Lila, a love-struck Writer, in the short-lived E4 series Nearly Famous (2007). She plays Angela in the 2016 television series Westworld.

Riley made her stage debut in The Philadelphia Story at the Old Vic in 2005. Her performance in a 2006 revival of Tennessee Williams' Summer and Smoke was described by critic Rachel Read as being "delightful".

In 2008, Riley began dating Billionaire Entrepreneur Elon Musk and in 2010 they married at Dornoch Cathedral. In January 2012, Musk announced that he had ended his four-year relationship with Riley. In March 2012, Musk was seeking a divorce.

She was featured on the March 2010 cover of Esquire.

In 2011, she was named a "Brit to Watch" by the British Academy of Film and Television Arts.

However, in July 2013, Musk and Riley remarried. In a 60 Minutes interview in 2014, the couple stated that they had reconciled and were living together again, along with Musk's five children from his first marriage to Writer Justine Musk. On 31 December 2014, the Associated Press reported that Musk had filed for divorce; however the action was withdrawn. It was reported that Riley had been living separately from Musk for six months and filed for a second divorce in Los Angeles Superior Court on 21 March 2016. The divorce was finalised in October 2016.