During the 1960s, Peil toured with Boris Goldovsky's opera company and the Metropolitan Opera's national company singing such roles as Susanna in Mozart and da Ponte's The Marriage of Figaro. She also sang with the New York City Opera.

In 1971, she originated the role of Alma in the opera Summer and Smoke, based on a Tennessee Williams play, and performed it again when it was broadcast on television in 1982 (based on a 1980 performance). Peil was persuaded to take a role in Kiss Me, Kate and soon found herself on Broadway. In May 1983 she was cast in a national tour as the twelfth and final Anna Leonowens opposite Yul Brynner's monarch of Siam in a revival of The King and I. The production toured the United States, closing on Broadway shortly before Brynner's death in 1985. Peil was nominated for a 1985 Tony Award for Best Performance by a Featured Actress in a Musical.She starred in the 1987 Off-Broadway musical Birds of Paradise. She made her film debut in 1992's Jersey Girl. She appeared on TV's Law & Order in 1994. Peil won an Obie Award in 1995 for her work in three non-musical plays, The Naked Truth, Missing Persons, and A Cheever Evening.

Between 1998 and 2003, Peil was introduced to a wider audience through her role as Evelyn 'Grams' Ryan on teen television drama Dawson's Creek. Alongside the four main young stars of that show, she was the only actress to appear as a credited regular throughout the show's six-season run, appearing in 74 of 128 episodes. From 2009 to 2016, she played Jackie Florrick, the mother of Chris Noth's character, on the CBS drama The Good Wife.

Starting in October 2010 she appeared in the original Broadway cast of the Lincoln Center Theater production of the musical Women on the Verge of a Nervous Breakdown, which is based upon the movie of the same name. The show had a limited run until January 2011. Peil appeared in Stephen Sondheim's Follies on Broadway in the role of Solange LaFitte, alongside Bernadette Peters and Elaine Paige, starting in August 2011. In March 2012, she appeared as Erica Morini in Willy Holtzman's off-Broadway play The Morini Strad about the concert violinist.

In 2017, Peil received a Tony Award nomination for Best Featured Actress in a Musical for her role in Anastasia.

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