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A graduate of San Francisco State University and the American Conservatory Theater, Bening started her career on stage with the Colorado Shakespeare Festival company in 1980, and played Lady Macbeth in 1984 at the American Conservatory Theater. She made her Broadway debut in the Tina Howe play Coastal Disturbances (1987), for which she received a nomination for the Tony Award for Best Featured Actress in a Play. Making her film debut in 1988, she gained further recognition for her role in The Grifters (1990), for which she received her first Academy Award nomination. This acclaim continued throughout the 1990s and 2000s with further Oscar-nominated performances in the comedy-dramas American Beauty (1999) and Being Julia (2004), which respectively won her the BAFTA and Golden Globe for Best Actress. Bening's performance as the title character in the British television film Mrs. Harris (2005) earned her a nomination for the Primetime Emmy Award for Outstanding Lead Actress in a Miniseries or Movie.

In the following decades, Bening received two additional Oscar nominations for her leading roles as a lesbian mother in The Kids Are All Right (2010) and swimmer Diana Nyad in the Netflix biographical film Nyad (2023), the former of which also won her a Golden Globe. She returned to Broadway in the revival of Arthur Miller's All My Sons (2019), earning another Tony nomination for Best Actress in a Play. Her other roles during this period include the films 20th Century Women (2016), Film Stars Don't Die in Liverpool (2017), Captain Marvel (2019), and Death on the Nile (2022), and the miniseries Apples Never Fall (2024).