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Her next role was in the HBO television film If These Walls Could Talk 2 (2000), a drama about three lesbian couples in different time periods.
Williams agreed to the part after ensuring that a sex scene between Chloë Sevigny and her was pertinent to the story and was not meant to titillate.
She next took on guest roles in the television sitcoms Step by Step and Home Improvement, and appeared in the brief part of Sil, a character played in adulthood by the actress Natasha Henstridge, in the 1995 science fiction film Species.
In 1997, unhappy with the roles she was being offered, Williams collaborated with two other actresses to write a script named Blink, about prostitutes living in a Nevada brothel, which despite being sold to a production company was never made.
In a review of the first season for The New York Times, Caryn James called it a soap opera that was "redeemed by intelligence and sharp writing" but thought that Williams was "too earnest to suit this otherwise shrewdly tongue-in-cheek cast".
Her first film release since the start of Dawson's Creek was Halloween H20: 20 Years Later (1998), a slasher film starring Jamie Lee Curtis.
The following year, she made her film debut in the family movie Lassie, about the bond between a young boy (played by Tom Guiry) and the titular dog.
Her first screen appearance was as Bridget Bowers, a young woman who seduces Mitch Buchannon's son, Hobie, in a 1993 episode of the television series Baywatch.
Despite significant media attention, Williams is reticent about her personal life.
She has a daughter from her relationship with the late actor Heath Ledger, and she is separated from the musician Phil Elverum, whom she married in 2018.
Williams went on to gain critical acclaim for playing emotionally troubled women coping with loss or loneliness in the independent dramas Wendy and Lucy (2008), Blue Valentine (2010), and Manchester by the Sea (2016).
For her portrayal of Marilyn Monroe in My Week with Marilyn (2011), she won a Golden Globe Award for Best Actress.
For playing a sexually abused woman in Blackbird, she received a nomination for the Tony Award for Best Actress in a Play.