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After graduating from the Royal Academy of Dramatic Art, she started her career as a stage actress in productions such as Romeo and Juliet (playing Juliet), Much Ado About Nothing, and A Midsummer Night's Dream. Her first major role was in Mike Leigh's All or Nothing in 2002. She continued working with Leigh, appearing in a supporting role in Vera Drake (2004) and taking the lead in Happy-Go-Lucky (2008), for which she won several awards, including the Golden Globe Award for Best Actress in a Motion Picture – Musical or Comedy and the Silver Bear for Best Actress.

Hawkins appeared in two Woody Allen films, Cassandra's Dream (2007) and Blue Jasmine (2013); for the latter, she received an Academy Award nomination for Best Supporting Actress. She went on to play lead roles in Made in Dagenham (2010), Paddington (2014), Maudie (2016), and Paddington 2 (2017). She appeared in Godzilla (2014), Godzilla: King of the Monsters (2019) and Wonka (2023). For starring as Elisa Esposito, a mute cleaning woman in the fantasy film The Shape of Water (2017), she earned critical acclaim. She was nominated for the Academy Award for Best Actress.

She has also appeared in stage productions with the Royal Court Theatre in London, and in 2010 made her Broadway debut in Mrs. Warren's Profession. In 2012, she starred in Constellations at the Royal Court Theatre, which later moved to the Duke of York's Theatre in the West End. On television, she appeared in the BBC adaptations of Tipping the Velvet (2002) as Zena Blake and Fingersmith (2005) as Sue Trinder. She also appeared as Anne Elliot in Persuasion (2007), ITV's adaptation of Jane Austen's novel. In 2025, Hawkins appeared in Bring Her Back, an Australian supernatural horror film directed by Danny and Michael Philippou.