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Blunt made her acting debut in the 2001 drama production of The Royal Family and portrayed Catherine Howard in the television miniseries Henry VIII (2003). She made her feature film debut in the drama My Summer of Love (2004). Blunt's breakthrough came in 2006 with her starring roles in the television film Gideon's Daughter and the comedy-drama The Devil Wears Prada. The former won her a Golden Globe Award for Best Supporting Actress. Her profile continued to grow with leading roles in the period film The Young Victoria (2009), the romantic comedy Salmon Fishing in the Yemen (2011), the science fiction films The Adjustment Bureau (2011), Looper(2012) and Edge of Tomorrow (2014), and the musical Into the Woods (2014).

Blunt received critical acclaim for playing an idealistic FBI agent in the crime film Sicario (2015), an alcoholic in the psychological thriller The Girl on the Train (2016), and a survivalist mother in her husband John Krasinski's horror film A Quiet Place (2018), for which she won a SAG Award for Best Supporting Actress. She has since starred in the sequels Mary Poppins Returns (2018) and A Quiet Place Part II (2021), the fantasy adventure Jungle Cruise (2021), and the revisionist Western television miniseries The English (2022). Her portrayal of Katherine Oppenheimer in Christopher Nolan's biographical thriller film Oppenheimer (2023) earned her a nomination for the Academy Award for Best Supporting Actress.

Blunt has been working with the American Institute for Stuttering since 2006 to help children overcome stuttering through educational resources and raise awareness of the realities of the condition. She is on the institute's board of directors and hosts a gala to raise funds for speech therapy scholarships for children and adults.