She is best known for originating the roles of Barbara Maitland in Beetlejuice, Penny Pingleton in Hairspray, and Clio/Kira in Xanadu, the latter of which earned her a Tony Award nomination for Best Performance by a Leading Actress in a Musical.

Other New York roles included Vicky Hollins in the workshop of Bright Lights, Big City, Barrow in The "I" Word and Claudia in The Folsom Head.

In 1995, Butler originated the role of Belle for the Toronto production of Disney's Beauty and the Beast, and she was nominated for a Dora Mavor Moore Award for Best Leading Actress for her performance.

[7] In February 2002, Butler was cast as Penny Pingleton (a role she had originated in workshops) in Hairspray, the musical version of the John Waters 1988 film of the same name.

While Hairspray went into pre-production, Butler played the free-spirited performance artist Maddie in the limited run of the intimate Australian musical Prodigal at the York Theatre.

Butler revisited her long-lost childhood Brooklyn accent to play Audrey, the love interest with a sadistic dentist boyfriend Dr. Orin Scrivello and a heart of gold.

[11] A fan of Little Shop composer Alan Menken,[12] who also wrote the music for Beauty and the Beast, Butler received an Outer Critics Circle nomination for her performance.

After leaving the show in the summer of 2004, Butler traveled to San Francisco where she created the role of scheming, foul-mouthed teenager Dedee Truitt in the new musical The Opposite of Sex, which had its world premiere at the Magic Theatre that fall.

[17] In February and March 2008, Butler appeared as Reese, the thieving assistant to fashion designer Victory Ford (Lindsay Price), in the first season of the television series Lipstick Jungle on NBC.

The album is entitled Faith, Trust & Pixie Dust and features some of Butler's favorite songs from Disney films and shows given "intimate, acoustic" arrangements.

Of note is the track "This Only Happens in the Movies", an unreleased song written by Alan Menken (for the unrealized prequel to Who Framed Roger Rabbit), being given its inaugural recording.

The following month, she appeared on the ABC series Cupid as Debbie, a working-class masseuse who attempts to improve herself to impress her wealthy boyfriend Lance Stillwell (Paul Fitzgerald).

[22] She played the lead role of Sherrie Christian, a small-town girl who moves to the Sunset Strip in Los Angeles to pursue her dream of becoming an actress.

In April 2010, Butler made her New York City cabaret debut at Feinstein's at the Regency with a show of songs she has performed on Broadway as well as personal favorites.

[24][25] Also in September 2011, Butler appeared on the series finale of FX's Rescue Me as Marsha, an overprotective mother who argues with Denis Leary's character Tommy Gavin on a playground.

The production costarred Angela Lansbury, James Earl Jones, Candice Bergen, Eric McCormack, John Larroquette, Michael McKean, and Jefferson Mays.

From March through May 2013, Butler appeared Off-Broadway in The Call, a new play by Tanya Barfield, a co-production between Playwrights Horizons and Primary Stages.

In May 2013, Butler appeared on an episode of Law and Order: Special Victims Unit as Ariel Randolph, a mother with a secret life whose bad decisions have tragic consequences.

In October 2015, Butler made her solo debut at Feinstein's/54 Below with Seth Rudetsky on piano, performing hits from her career as well as telling behind-the-scenes stories.

[30] She played Marianne Wilson, a career-oriented reporter who, while investigating the story of a poorly constructed casino ship, runs into an unexpected person from her past.

The Hollywood Reporter noted her role as "...stand-in from the movie, sardonic math teacher Ms. Norbury, played here by Kerry Butler, acing triple-duty with distinctive takes also on Cady's earnest mother and Regina's self-described 'cool mom'".

'"[36] From October to November 2018, Butler appeared in the world premiere of the musical Beetlejuice at the National Theatre in Washington, D.C., in the role of Barbara Maitland.

[41] In January 2024, Butler appeared with her original Hairspray costars Laura Bell Bundy and Marissa Jaret Winokur in Mama, I'm a Big Girl Now!, a concert the three of them conceived, wrote, and directed.