In 1997, Ambrose made her feature debut in the Frank Oz comedy "In and Out" playing Vickie Rayburn, a gifted student of Kevin Kline's sexually ambiguous English teacher. More screen time came with her turn in the following year's "Can't Hardly Wait". She played quick-witted recluse Denise in this graduation party-set ensemble comedy, best friend of lovestruck Preston (Ethan Embry) and unlikely love match for hip-hop wannabe Kenny (Seth Green). The film was a hit with the teen set, and Denise emerged as a most relatable and realistic character, due in no small part to the actress' spot-on cynical portrayal. Already a familiar face to the series' core audience, Ambrose took on a well-received 1999 recurring role on Fox's "Party of Five" playing Myra, a troubled teen who escapes her personal problems through alcohol and irresponsible sexual activity and fabricates a story about the Salingers' pseudo-patriarch Charlie (Matthew Fox) that threatens to ruin his career. The actress' nuanced and morally ambiguous take on the character elevated Myra from typical two-dimensional misunderstood bad girl to an interesting individual.

Ambrose proved an engaging screen presence and talented performer with promising starring turns in the independent films "Swimming" (1999) and "Psycho Beach Party" (2000). In the former, a thoughtful coming-of-age drama, she starred as a shy tomboy in a seaside resort town who spends her summer fascinated with an inspiring blonde free spirit (Joelle Carter) and involved with a mysterious and enchanted drifter (Jamie Harrold). As the film's central character, Ambrose showed a unique ability for eliciting audience empathy, emerging as a dynamic Everywoman. The campy comedy "Psycho Beach Party" allowed her to showcase not only her sense of humor but her musical gifts as well, playing a teenage introvert turned popular surfer chick with multiple personality disorder in this wacky beach party murder mystery based on Charles Busch's popular Off-Broadway play. She returned to television in the HBO black comedy "Six Feet Under" (2001-2005). Written, produced and directed by "American Beauty" scripter Alan Ball, the series followed a family that runs a funeral parlor, with Ambrose starring as the family's young daughter Claire, a tart-tongued, anti-authoritarian aspiring artist who frequently questions societal conventions. In 2002, Amborse was nominated for an Emmy award for her authentic, uncompromising portrayal.