Columbia Tri-Star Television, producer of a new show named Dawson's Creek that was created by screenwriter Kevin Williamson, asked her to come to Los Angeles to audition, but there was a conflict with her schedule. The film was recut from what the director intended.Roger Ebert of the Chicago Sun-Times wrote her character, Rachel, "dresses in black and likes to strike poses on the beds of pickup trucks and is a bad girl who is in great danger of becoming a very good one." Despite the fact that it received mixed reviews and was not a huge financial success, the actress won a MTV Movie Award for Best Breakthrough Performance for the role and also received a Saturn Award nomination for the part.
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She has also played on Broadway in a production of Arthur Miller's All My Sons, and had numerous guest roles on television programs such as How I Met Your Mother.
In 2011, she starred as Jacqueline Kennedy in The Kennedys miniseries, a role she reprised in the 2017 miniseries The Kennedys: After Camelot.
Todd Mc Carthy of Variety and Roger Ebert commended her performance, During the final season of Dawson's Creek, Holmes played the mistress of the public relations flack played by Colin Farrell in Phone Booth, which was both critically and financially successful.
She also appeared as Robert Downey, Jr.'s nurse in The Singing Detective (2003).
In January 1997, Holmes went to Los Angeles for pilot season, when producers cast and shoot new programs in the hopes of securing a spot on a network schedule. I thought, 'There is no way I'm not playing Lola to go audition for some network. Jancee Dunn, an editor at Rolling Stone said she was chosen for the cover because "every time you mention Dawson's Creek you tend to get a lot of dolphin-like shrieks from teenage girls.
The Toledo Blade reported she was offered the lead in Buffy the Vampire Slayer but she never turned it down. The fact that she is drop-dead gorgeous didn't hurt either." During her time as a series regular on Dawson's Creek, Holmes first leading role in a film came in 1998's Disturbing Behavior, a Scream-era Stepford Wives-goes-to-high school thriller, where she was a loner from the wrong side of the tracks.
Holmes had a small role (six and one-half minutes of screen time) as Hannah Green, the talented student who lusts after Professor Grady Tripp (Douglas's character, who is her instructor and landlord).
Many leading critics at the time took favorable notice to Holmes in the film.
The first was in Wonder Boys, directed by Curtis Hanson from the novel by Michael Chabon.
The film told the story of a creative writing teacher at a university, with Michael Douglas in the leading role.
Dawson's Creek ended its run in 2003, and Holmes was the only actor to appear in all 128 episodes.