Jones was born in Paris, Tennessee. Her mother was a high school Teacher and her father owned a flower shop. Her parents were very supportive of her theatrical ambitions, encouraging her interest by sending her to classes with local drama Teacher, Ruby Krider. Jones takes great pains to credit her high school speech Teacher, Linda Wilson, with her first real preparatory work. She is a 1978 graduate of the Carnegie Mellon School of Drama. While at CMU, she was one of the earliest actors to work at City Theatre, a prominent fixture of Pittsburgh theatre.
Jones made her Broadway debut in the 1987 original Broadway production of Stepping Out. Other stage credits include Pride's Crossing (1997–98) and The Glass Menagerie (2013–14). Her film appearances include The Horse Whisperer (1998), Erin Brockovich (2000), The Village (2004), Amelia (2009) and The Beaver (2011). In 2012, she played Dr. Judith Evans on the NBC drama Awake.
Jones is openly lesbian. In 1995, when Jones accepted her first Tony Award, she thanked her then-partner, Architect Mary O'Connor, with whom she had an 18-year relationship.
Other Broadway credits include Nora Ephron's play Imaginary Friends (with Swoosie Kurtz), the 2000 revival of A Moon for the Misbegotten, and Timberlake Wertenbaker's Our Country's Good, for which she earned her first Tony nomination. She is considered to be one of the foremost theater actresses in the United States. In 1994, she also appeared in the Broadway run of Angels in America: Millennium Approaches and Perestroika as the Angel, replacing Ellen McLaughlin who had originated the role.
She started dating Actress Sarah Paulson in 2004. When she accepted her Best Actress Tony in 2005 for her work in Doubt, she thanked "Laura Wingfield," the Glass Menagerie character being played in the Broadway revival by Paulson. In 2007, Paulson and Jones declared their love for each other in an interview with Velvetpark at Women's Event 10 for the LGBT Center of New York. Paulson and Jones ended their relationship amicably in 2009.
Also in 2012, she portrayed Amanda Wingfield in the Loeb Drama Center's revival of Tennessee Williams' The Glass Menagerie alongside Zachary Quinto, Brian J. Smith and Celia Keenan-Bolger.
In 2014, Cherry Jones was inducted into the American Theater Hall of Fame.
In mid-2015, Jones married her girlfriend, filmmaker Sophie Huber.
In 2016, she appeared in "Nosedive", an episode of the anthology series Black Mirror.
In 2018, Jones will be playing Holly, the feminist mother to June/Offred in The Handmaid's Tale who has only been mentioned in passing during flashback scenes. She will appear in episode three.
