Initially hoping to study philosophy at University of Cambridge, for which she secured a place, Myles instead turned to acting after television writer Julian Fellowes saw her perform in a school play, casting her in his series The Prince and the Pauper (1996).

Her mother, Jane (née Allan), works in educational publishing, and her father, Peter R. Myles, was a retired Church of England vicar in Isleworth, West London.

Following success at her A Levels she secured a place at the University of Cambridge to study philosophy, but chose to pursue an acting career after being spotted by Julian Fellowes in a school play and shortly after had a small role in his television production of The Prince and the Pauper in 1996.

[6] Myles also had roles as Gwenda Halliday in the British detective drama Agatha Christie's Marple: Sleeping Murder and Sophie Amsden in American thriller Covert One: The Hades Factor on television before starring in the 2006 comedy film Art School Confidential.

In 2008, she played Freya, the daughter of John Hurt's character, in the sci-fi action epic Outlander with Jim Caviezel and Ron Perlman.

In 2014, Myles starred as geologist Darcy Tirrel opposite Mark Wahlberg and Stanley Tucci in the sci-fi action blockbuster Transformers: Age of Extinction which was directed by Michael Bay and produced by Steven Spielberg.

[10] Later in 2014, Myles starred as Rachel in the psychological horror film Blackwood before going on to have roles as Dr. Anna Clarke in the international action-thriller Crossing Lines and the aristocratic Lady Katherine Longmore in the miniseries Our Zoo.

[13] In 2021, Myles starred as Beth Barnes in the comedy-heist film Decrypted about the kidnap of the creator of Bitcoin, alongside Amanda Abbington and Kevin McNally.

In December 2021, Myles played Louise Campbell, Duchess of Argyll in the acclaimed BBC television mini-series A Very British Scandal with Claire Foy and Paul Bettany.