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She appeared as Margo Lane in The Shadow with Alec Baldwin, as well as in the film Miles from Home directed by Gary Sinise.

Miller co-starred as the daughter of the character played by Marlon Brando in 1990's The Freshman, again opposite Matthew Broderick, and as the lawyer and stepdaughter of the character played by Gregory Peck in 1991's Other People's Money.

She subsequently appeared in a number of other theatrical movies, notably as Edna Purviance in Chaplin and with Tim Daly as Margaret 'Maggie' Harwood in Peter Yates' film Year of the Comet, both in 1992, and the following year she appeared as the love interest of Al Pacino's character in Carlito's Way. She also appeared in the 1990 movies Downtown, with Anthony Edwards and Forest Whitaker, and Kindergarten Cop, alongside Arnold Schwarzenegger, playing a teacher, hiding with her son Dominic from her criminal drug-dealing husband Cullen Crisp ( Richard Tyson). In 1990, she played Paula in Awakenings, starring Robert De Niro and Robin Williams. She played a supporting role in 1989's ' Dead Bang', a cop thriller starring Don Johnson. She then appeared as Pee-wee Herman's ( Paul Reubens) fiancée, Winnie Johnston, in the 1988 release of Big Top Pee-wee. She then returned to Broadway in a revival of Our Town her portrayal of Emily garnered her a Tony award nomination.

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She played a role in one episode ('Death and the Lady') of the television series Miami Vice (which aired on October 16, 1987), and accepted several other small roles in film and television work. (She also starred with Broderick in the 1988 film version of that play). Her Broadway theatre break came in 1985 when she was cast in the lead (opposite Matthew Broderick) in the Neil Simon play Biloxi Blues. Miller graduated from high school in Los Angeles and attended Menlo College in Atherton, California for two years from 1981 to 1983, then moved to New York City to study theatre at HB Studio. She has two sisters: older, Marisa Miller, who is also a film actress, and younger, Savannah Miller, a social worker. Her mother was the goddaughter of businessman Aristotle Onassis and an editor of Harper's Bazaar. Miller was born in Los Angeles, California, to Beatrice (née Ammidown), a costume designer, publicist, and journalist, and Mark Miller, a television actor and producer. Miller's other films include a starring role in The Relic (1997) and supporting roles in Chaplin (1992), Along Came a Spider (2001), and The Artist (2011). She returned to Broadway in the 1995 original stage production of On the Waterfront. She has appeared in several major Hollywood films, particularly in the late 1980s and early 1990s, including Adventures in Babysitting (1987), Biloxi Blues (1988), Big Top Pee-wee (1988), The Freshman (1990), Awakenings (1990), Kindergarten Cop (1990), Other People's Money (1991), Year of the Comet (1992), and Carlito's Way (1993), for which she received a Golden Globe Award nomination. She began her career on Broadway in the 1985 original production of Biloxi Blues and received a Tony Award nomination for the 1989 revival of Our Town. Penelope Ann Miller (born Penelope Andrea Miller January 13, 1964), sometimes credited as Penelope Miller, is an American actress.