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Madigan made her film debut in the drama Love Child (1982), for which she was nominated for the Golden Globe Award for New Star of the Year – Actress. For playing a woman in a difficult marriage in the drama film Twice in a Lifetime (1985), she earned a nomination for the Academy Award and Golden Globe Award for Best Supporting Actress. She has also acted in Love Letters (1984), Alamo Bay (1985), Nowhere to Hide (1987), Uncle Buck (1989), Field of Dreams (1989), Female Perversions (1996), Pollock (2000), and Gone Baby Gone (2007). After a lack of "meaningful roles", she gained newfound attention for her performance in the horror film Weapons (2025).

On television, Madigan portrayed Sarah Weddington in the television film Roe vs. Wade (1989), for which she won the Golden Globe Award and was nominated for a Primetime Emmy Award. She also took roles in the HBO series Carnivàle (2003–2005), Grey's Anatomy (2008–2009), and Fringe (2009). On stage, she has acted in the Off-Broadway production of The Lucky Spot (1987), for which she was nominated for the Drama Desk Award for Outstanding Actress in a Play, and a 1992 Broadway production of A Streetcar Named Desire in the role of Stella Kowalski.