During this time, Witt supported herself by playing piano at the Regent Beverly Wilshire Hotel. She went on to play small parts in Mike Figgis' Liebestraum (in which her brother Ian also appears), the Gen-X drama Bodies, Rest & Motion and the TV movie The Disappearance of Vonnie. In 1994, the red-haired Witt landed her first lead role in a film, playing a disturbed teenager in Fun. She received the Special Jury Recognition Award at the Sundance Festival and was nominated for Best Actress at the Independent Spirit Awards. This performance inspired Madonna to recommend Witt to be cast as her daughter in the first segment, "The Missing Ingredient" of Four Rooms. Witt was introduced to a larger audience playing the role of Zoey Woodbine, daughter of actress Cybill Shepherd's character in the sitcom Cybill from 1995 to 1998. Between seasons she starred in films: Mr. Holland's Opus, Alexander Payne's abortion comedy Citizen Ruth, Passion's Way and Bongwater. After Cybill was cancelled, Witt received a leading role in the horror film Urban Legend and the animated feature Gen which was never released because the studio stopped funding before the completion of the movie.

In 2000, Witt had starring roles on the television shows Ally McBeal and The Sopranos; the lead role in the comedy Playing Mona Lisa, a supporting part in John Waters' Cecil B. Demented, and her stage debut in Robbie Fox's musical The Gift at the now-closed Tiffany Theater in Los Angeles, in which she played a high-priced stripper with a disease. In the years following, Witt's acting career slowed. She had a small part in Cameron Crowe's Vanilla Sky, which was intended as a reference to her roles in Dune and Liebestraum. She also played a college graduate who discussed losing her virginity in the experimental Ten Tiny Love Stories and the trailer-trash "Barbie" in American Girl, which was released to video in 2005.

She appeared in the 2002 romantic comedy Two Weeks Notice opposite Hugh Grant. In 2003-2004, she lived primarily in the UK, filming The Upside of Anger opposite Kevin Costner; and she starred as Evelyn in a stage-production of Neil LaBute's The Shape of Things. Between these two projects, she went to South Africa to shoot the German TV movie Kingdom in Twilight which also goes by the names The Sword of Xanten and The Ring of the Nibelungs. She played Kriemhild in this film interpretation of the epic poem Das Nibelungenlied, which was released in the US as Dark Kingdom: The Dragon King. On June 14, 2004, Witt modeled what is believed to be the most expensive hat ever made, for Christie's auction house in London. The Champrau d'Amour, designed by Louis Mariette, is valued at $2.7 million (US) and is encrusted in diamonds. In September 2006 she returned to the London stage, portraying the piano-playing Abigail, a role in which she demonstrated herself an "outstanding" pianist, in Piano/Forte at the Royal Court Theatre. Witt joined the cast of Law & Order: Criminal Intent for the 2007-08 season as Det. Nola Falacci, a character who is a temporary replacement for Megan Wheeler, played by Julianne Nicholson who was away on maternity leave.

• "Law & Order: Criminal Intent" .... Detective Nola Falacci / ... (7 episodes, 2007-2008)
  ... aka Law & Order: CI (USA: promotional abbreviation)
       - Episode #8.3 (2008) TV episode .... Det. Nola Falacci
       - The Glory That Was... (2008) TV episode .... Det. Nola Falacci
       - Senseless (2007) TV episode .... Detective Nola Falacci
       - Offense (2007) TV episode .... Detective Nola Falacci
       - Courtship (2007) TV episode .... Detective Nola Falacci
        (2 more)
• "Two and a Half Men" .... Miss Pasternak (1 episode, 2008)
       - A Jock Strap in Hell (2008) TV episode .... Miss Pasternak
• "Wainy Days" .... Laura (1 episode, 2008)
       - Shelly II (2008) TV episode .... Laura
• 88 Minutes (2007) .... Kim Cummings
  ... aka 88 Minutes (International: English title) (USA: promotional title)
  ... aka 88 (USA: closing credits title)
  ... aka 88: 88 Minutes (USA: complete title)
• Blue Smoke (2007) (TV) .... Reena Hale
  ... aka Nora Roberts' Blue Smoke (USA: complete title)
• Last Holiday (2006) .... Ms. Burns
• The Upside of Anger (2005) .... Hadley Wolfmeyer
  ... aka An deiner Schulter (Germany)
• Ring of the Nibelungs (2004) (TV) .... Kriemhild
  ... aka Curse of the Ring (Australia: DVD title) (International: English title) (USA: DVD title)
  ... aka Dark Kingdom: The Dragon King (USA: DVD title)
  ... aka Die Nibelungen (Germany)
  ... aka Die Nibelungen - Der Fluch des Drachen (Germany: DVD title)
  ... aka Saga dei Nibelunghi, La (Italy)
  ... aka Sword of Xanten (UK: theatrical title)
• Girls' Lunch (2004)
• "The Twilight Zone" .... Liz (1 episode, 2003)
       - The Executions of Grady Finch (2003) TV episode .... Liz
• Two Weeks Notice (2002) .... June Carver
• American Girl (2002/I) .... Barbie
  ... aka Confessions of an American Girl (USA: video title)
• Vanilla Sky (2001) .... Libby