Lister-Jones was born in Brooklyn, New York City. Her mother is the Canadian-born and New York-based video artist Ardele Lister, and her father is the American photographer and media artist Bill Jones. Her mother was born to a Jewish family, whereas her father converted to Judaism. In 2000, she graduated from Edward R Murrow High School in Brooklyn. She graduated with honors from the Tisch School of the Arts at New York University and studied at the Royal Academy of Dramatic Arts in London. Lister-Jones performed with a rock band. Her mother was president of a local Conservative egalitarian synagogue that the family attended every Saturday, and she also kept a kosher home.
Her debut solo CD was titled Skip the Kiss. Kyle Forester, who composed the score for Breaking Upwards, arranged the music for Skip the Kiss.
Lister-Jones' New York City theater credits include Seminar, The Little Dog Laughed and The New Group's The Accomplices. Her screen credits include the political thriller State of Play, Salt, The Other Guys, The Marconi Bros., Day Zero, as well as quirky independent films such as Armless, Arranged, and Palladio. On television she has appeared in Law & Order, Law & Order: Criminal Intent, Law & Order: SVU, Law & Order: Trial by Jury, on HBO's Bored to Death, as Kim on Adult Swim's Delocated, as Lily in the cast of the NBC sitcom Whitney, as Kate in Friends with Better Lives, as Councilwoman Fawn Moscato in New Girl, as Jen in Life in Pieces and as Carolyn Hart in the HBO film Confirmation.

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