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Jones made her Broadway debut in the 1987 play Stepping Out. She went on to receive two Tony Awards for Best Actress in a Play for The Heiress in 1995 and Doubt in 2005. Her other Tony-nominated roles were in Our Country's Good in 1991, A Moon for the Misbegotten in 2000, and The Glass Menagerie in 2014. Her most recent Broadway performance was in The Lifespan of a Fact in 2018.

She is also known for her work on television with breakthrough roles as Barbara Layton in The West Wing and President Allison Taylor in 24 the latter of which won her the Primetime Emmy Award for Outstanding Supporting Actress in a Drama Series in 2009. She received a Screen Actors Guild Award nomination for Transparent in 2015 and earned two Primetime Emmy Awards Outstanding Guest Actress in a Drama Series for her roles in the Hulu drama series The Handmaid's Tale in 2019 and the HBO drama series Succession in 2020.

Her film appearances include The Horse Whisperer (1998), Erin Brockovich (2000), Signs (2002), The Village (2004), Amelia (2009), The Beaver (2011), A Rainy Day in New York (2019), and The Eyes of Tammy Faye (2021).