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Her early films include Greystoke: The Legend of Tarzan, Lord of the Apes (1984) and the Brat Pack vehicle film St. Elmo's Fire (1985). Her breakout role was in Sex, Lies, and Videotape (1989), which earned her the Independent Spirit Award for Best Female Lead and a  Golden Globe nomination for Best Actress – Motion Picture Drama. She then starred in a series of films, including Green Card (1990), Groundhog Day (1993), Short Cuts (1993), Four Weddings and a Funeral (1994), Unstrung Heroes (1995), Michael (1996), Multiplicity (1996), and The Muse (1999).

MacDowell played supporting film roles in Beauty Shop (2005), Footloose (2011), Magic Mike XXL(2015), The Last Laugh (2019), Ready or Not (2019), The Other Zoey (2024) and Red Right Hand (2024). She starred in several independent films, most notably Love After Love (2017). She co-starred opposite her daughter, Margaret Qualley, in the Netflix miniseries Maid (2021), for which she was nominated for a Golden Globe Award. In 2023, MacDowell began starring in the Hallmark Channel fantasy drama series The Way Home.