She first became involved with the theatre when she was cast in a school production of Harvey. She refused to solicit acting tips and advice from her famous relatives, and studied method acting at New York University's Tisch School of the Arts and the Lee Strasberg Theatre Institute.

She made her film debut as an extra in the 1969 movie Easy Rider as a child in the hippie commune that Peter Fonda and Dennis Hopper visit on their trek across the United States. Her second film role was also a non-speaking role in the 1982 comedy Partners. It was not until 1988 that she had her first speaking role in a feature film starring with John Hurt in Scandal, based on the Profumo affair. That year, she also appeared in both You Can't Hurry Love and Shag.

Her first big role in a movie was when she starred as an attractive journalist in The Godfather, Part III. After gaining additional work experience on a few theater productions and small movie roles, she was cast in the lead for Barbet Schroeder's Single White Female. A review in the New Yorker proclaimed she had "...a provocative, taunting assertiveness" and Rolling Stone said that Fonda was "a comic delight". In 1997 Fonda was on the same flight as Quentin Tarantino and he offered her the part of a beach babe in Jackie Brown. Fonda was also offered the title role in Ally McBeal before Calista Flockhart, but turned it down to focus on her film career.

• Snow Queen (2002) (TV) .... Snow Queen
  ... aka Reine des neiges, La (Canada: French title)
• "The Chris Isaak Show" .... Stephanie Furst (4 episodes, 2002)
       - Wrong Number (2002) TV episode .... Stephanie Furst
       - Chris Isaak Day (2002) TV episode .... Stephanie Furst
       - The Devil Made Me Do It (2002) TV episode .... Stephanie Furst
       - In the Name of Love (2002) TV episode .... Stephanie Furst
• After Amy (2001) (TV) .... Linda Sanclair
  ... aka No Ordinary Baby (UK)
• The Whole Shebang (2001) .... Val Bazinni
• "Night Visions" .... Mary (1 episode, 2001)
       - The Occupant (2001) TV episode .... Mary
• Kiss of the Dragon (2001) .... Jessica Kamen
  ... aka Baiser mortel du dragon, Le (France)
  ... aka KOD: Kiss of the Dragon (USA: promotional abbreviation)
• Monkeybone (2001) .... Dr. Julie McElroy
• Delivering Milo (2001) .... Elizabeth
• South of Heaven, West of Hell (2000) .... Adalyne Dunfries
  
• Lake Placid (1999) .... Kelly Scott
  ... aka Lac Placid (Canada: French title)
• A Simple Plan (1998) .... Sarah Mitchell
  ... aka Ein Einfacher Plan (Germany)
  ... aka Un plan simple (France)
• Finding Graceland (1998) .... Ashley
• Break Up (1998) .... Jimmy Dade
  ... aka The Break Up (USA)
• Jackie Brown (1997) .... Melanie Ralston