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In her early career, Miller performed in several amateur New York City plays including The Striker, Independence, and Oscar-winning director Anthony Minghella's Cigarettes & Chocolate.

In 2001, she made her film début with South Kensington, with Rupert Everett and Elle Macpherson. Her next projects were High Speed and The Ride (aka Joy-Rider) in 2002. In 2003, Miller had a recurring role in Simon West's television action drama series Keen Eddie. Miller had a supporting role in the remake of the 1966 film Alfie starring Jude Law in 2004. In the same year, she made Layer Cake with Daniel Craig. In 2005, she made her professional stage début as Celia in a West End production of Shakespeare's As You Like It alongside Helen McCrory and Dominic West. She understudied the lead role of Rosalind, which she played for one performance, when McCrory fell ill.

Later that year, Miller played the female lead opposite Heath Ledger in the period drama, Casanova, followed by the role of 1960s socialite and Andy Warhol's muse Edie Sedgwick in the film Factory Girl, which opened December 29, 2006.

In 2007, Miller played Victoria, a small role opposite Michelle Pfeiffer and Robert De Niro in Matthew Vaughn's fantasy epic Stardust, based on the book by Neil Gaiman of the same name. That same year, she played an American starlet to Steve Buscemi's reporter in the film Interview, a remake of the Dutch movie with the same name. Later in 2007, she portrayed an undead bride opposite James Franco in the horror comedy Camille which did not receive a wide release and went to DVD shortly thereafter.

In 2008, Miller appeared in the film version of writer Michael Chabon's novel, The Mysteries of Pittsburgh, also starring Peter Sarsgaard and filmed The Edge of Love, with friend Keira Knightley, a biopic of Dylan Thomas in which she plays his wife Caitlin.

She appeared in the 2009 live-action film adaptation of the comic book and cartoon G.I. Joe, G.I. Joe: The Rise of Cobra, playing The Baroness. The film grossed $54 million in the United States during its opening weekend. That same year, Miller starred in the Comic Relief spoof of the film Mamma Mia! alongside English comediennes Dawn French and Jennifer Saunders.

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