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The actress next appeared in Imaginary Heroes, a drama about a family coping with their son's suicide, and played an impressionable young woman fixated on mental health in the period film A Hole in One.
Williams returned to the comedic genre with The Baxter, in which she played a geeky secretary.
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.
She performed in an amateur production of the musical Annie, and her parents would drive her from San Diego to Los Angeles to audition for parts.
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.
Williams played Holly, an insecure bibliophile, a part that came close to her personality.
The seventh installment in the Halloween film series, it featured Williams as one of several teenagers traumatized by a murderer.
Williams has credited Dawson's Creek as "the best acting class", but also admitted that she had not fully invested herself in it as "my taste was in contradiction to what I was doing every single day".
For playing a sexually abused woman in Blackbird, she received a nomination for the Tony Award for Best Actress in a Play.
Williams returned to television in 2019 to portray Gwen Verdon in the biographical miniseries Fosse/Verdon, receiving a nomination for a Primetime Emmy Award for Outstanding Lead Actress.