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Spencer made her film debut in the 1996 drama A Time to Kill. Following a decade of brief roles in film and television, her breakthrough came in 2011 when she played a maid in 1960s America in the drama film The Help, which won her the Academy Award for Best Supporting Actress. In ensuing years, she won the National Board of Review Award for Best Supporting Actress for her role in Ryan Coogler's biopic Fruitvale Station (2013), had a recurring role in the CBS sitcom Mom (2013–2015), and starred in the Fox drama series Red Band Society (2014–2015).

Spencer's roles as other black women in 1960s America, as Dorothy Vaughan in the biopic Hidden Figures (2016) and a cleaning woman in the fantasy The Shape of Water (2017), earned her two consecutive nominations for the Academy Award for Best Supporting Actress, becoming the first black actress to achieve such feat, as well as the first, and to date only, to be nominated twice after winning. She has since starred in The Divergent Series (2015–16), The Shack (2017), Gifted (2017), Instant Family (2018), Luce (2019), Ma (2019), Onward (2020), and Spirited(2022). She led the Apple TV+ drama series Truth Be Told (2019–2023). She was nominated for the Primetime Emmy Award for Outstanding Lead Actress in a Limited Series or Movie for portraying Madam C. J. Walker in the Netflix miniseries Self Made (2020).

As an author, Spencer created the children's book series Randi Rhodes, Ninja Detective. She has published two books in the series: The Case of the Time-Capsule Bandit (2013) and The Sweetest Heist in History (2015).