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Buckley began her career in 2008 as a contestant on the BBC talent show I'd Do Anything, in which she came second. A RADA graduate, her early onscreen appearances were in BBC television series such as War & Peace (2016) and Taboo (2017). Buckley made her film debut with the lead role in Beast (2017), followed by her breakout role as an aspiring country music singer in the musical film Wild Rose (2018); the latter earned her a nomination for the BAFTA Award for Best Actress in a Leading Role.

Buckley's career progressed with starring roles in films such as I'm Thinking of Ending Things (2020), Men (2022), Women Talking (2022) and Wicked Little Letters (2023). For her performance as a troubled mother in the psychological drama The Lost Daughter (2021), she received nominations for the BAFTA Award for Best Actress in a Supporting Role and the Academy Award for Best Supporting Actress. She gained further recognition for her portrayal of Agnes Shakespeare in the period drama Hamnet (2025), receiving a Golden Globe, a BAFTA Award, an Actor Award, and the Academy Award for Best Actress.

On television, Buckley has starred in the HBO miniseries Chernobyl (2019) and season four of Fargo (2020). On stage, Buckley's portrayal of Sally Bowles in a 2021 West End theatre revival of Cabaret won her the Laurence Olivier Award for Best Actress in a Musical. In 2022, she released the collaborative album For All Our Days That Tear the Heart with Bernard Butler, which was shortlisted for the 2022 Mercury Prize.