Duff was born and raised in Hayes End, Middlesex by Irish parents. She attended Mellow Lane School, Hayes End, Hillingdon. She studied acting at The Drama Centre, now part of the University of the Arts London, having initially also applied to art colleges. Her father convinced her that she was not an artist and told her to persevere with acting. She took another year out after A-Levels before being accepted to The Drama Centre.

She is married to actor James McAvoy. They live in Stroud Green, London. She is a fan of Celtic Football Club.
In 2000, Duff was nominated for a Laurence Olivier Award, but first became well known as Fiona in the television programme Shameless, and for her portrayal of Elizabeth I of England in the lavish 2005 BBC television miniseries, The Virgin Queen.

An accomplished theatre actor, she has worked extensively with the Royal National Theatre and also in London`s West End (Vassa, Collected Stories). Theatre credits for the National Theatre include Collected Stories, King Lear, War and Peace and La Grande Magia. Her other theatre credits include The Soldier`s Fortune, Days of Wine and Roses, The Playboy of the Western World, The Daughter in Law and A Doll`s House.

Her film credits include French Film, Born Equal, Waiting Room, Garage, The Magdalene Sisters, Enigma and Mild and Bitter. Duff also made a cameo in film thriller Notes on a Scandal. She most recently played the title character in Marianne Elliott`s production of Bernard Shaw`s Saint Joan at the National Theatre to great acclaim

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