The daughter of Jacqui and Colin Hawkins, authors and illustrators of children's books, Hawkins was raised in Blackheath in southeast London, and attended James Allen's Girls' School in Dulwich. She then went on to study at the Royal Academy of Dramatic Art, graduating in 1998.

Hawkins' theatre appearances include Much Ado About Nothing (2000), A Midsummer Night's Dream (2000), Misconceptions (2001), Country Music (2004), and David Hare's adaptation of Federico García Lorca's The House of Bernarda Alba in 2005.

Hawkins made her first notable screen performance as Samantha in the 2002 Mike Leigh film All or Nothing. She also appeared as Slasher in the 2004 film Layer Cake. Her first major television role came in 2005 when she played Susan Trinder in the BAFTA-nominated BBC drama Fingersmith, an adaptation of Sarah Waters' novel of the same name, in which she co-starred with Imelda Staunton, as she had in Vera Drake. Since then she has gone on to star in another BBC adaptation, Patrick Hamilton's Twenty Thousand Streets Under the Sky.

Hawkins has appeared in three episodes of the hit BBC comedy series Little Britain, in addition to Ed Reardon's Week on BBC Radio 4. She also has contributed her writing and vocal skills to the BBC Radio 4 series Concrete Cow.

In 2006, Hawkins returned to the stage, appearing at the Royal Court Theatre in Jez Butterworth's The Winterling. In 2007, she played the lead in a new film of Jane Austen's Persuasion, and followed this with her critically-acclaimed performance in Happy-Go-Lucky.

Hawkins' upcoming films include Desert Flower, Never Let Me Go, and Happy Ever Afters. She is attached to work on a number of forthcoming films including Made in Dagenham and The Roaring Girl, in which she will play Bernadette Devlin.

At the 2007 Festival de Télévision de Monte-Carlo, Hawkins won the Golden Nymph for Best Performance by an Actress for her role as Anne Elliot in Persuasion.

In addition to the Golden Globe, Hawkins received numerous awards for her starring role in Happy-Go-Lucky, including the Silver Bear for Best Actress at the Berlin International Film Festival, the Boston Society of Film Critics Award for Best Actress, the Hollywood Film Festival Breakthrough Award, the Los Angeles Film Critics Association Award for Best Actress, the Mill Valley Film Festival Spotlight Award, the National Society of Film Critics Award for Best Actress, the New York Film Critics Circle Award for Best Actress, the San Francisco Film Critics Circle Award for Best Actress, the Santa Barbara International Film Festival Virtuoso Award, and the Satellite Award for Best Actress – Motion Picture Musical or Comedy.

Nicole Kidman (2001) · Renée Zellweger (2002) · Diane Keaton (2003) · Annette Bening (2004) · Reese Witherspoon (2005) · Meryl Streep (2006) · Marion Cotillard (2007) · Sally Hawkins (2008) · Meryl Streep (2009)

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