"Our beloved James David Van Der Beek passed peacefully this morning. He met his final days with courage, faith, and grace," Van Der Beek's family wrote in a statement posted to social media.
"There is much to share regarding his wishes, love for humanity and the sacredness of time. Those days will come.
"For now we ask for peaceful privacy as we grieve our loving husband, father, son, brother, and friend."
"While James' legacy will always live on, this is a huge loss to not just your family but the world," Sarah Michelle Gellar wrote on social media.
A GoFundMe was launched to raise $US500,000 ($A800,000) to help support Van Der Beek's widow and six children. It raised more than $US200,000 ($A280,000) less than an hour after being launched.
Van Der Beek revealed in 2024 he was being treated for colorectal cancer.
The actor made a surprise video appearance in September at a Dawson's Creek reunion charity event in New York City after previously dropping out due to illness.
A one-time theatre kid, Van Der Beek would star in the movie Varsity Blues and on TV in CSI: Cyber as FBI Special Agent Elijah Mundo, but was forever connected to Dawson's Creek, which ran from 1998 to 2003.
The series followed a high school group of friends as they learned about falling in love, creating real friendships and finding their footing in life.
Van Der Beek, than 20, played 15-year-old Dawson Leery, who aspired to be a director of Steven Spielberg quality.
Dawson's Creek, with the moody theme song Paula Cole's I Don't Want To Wait, was popular with teens and young adults who related to its hyper-articulate dialogue and frank talk about sexuality.
And it made household names of Van Der Beek, Joshua Jackson, Katie Holmes and Michelle Williams.
Van Der Beek sometimes struggled to get out from under the shadow of the show but eventually leaned into lampooning himself, like on Funny Or Die videos and on Kesha's Blow music video, which included his laser gun battle with the pop star in a nightclub and dead unicorns.
"It's tough to compete with something that was the cultural phenomenon that Dawson's Creek was," he told Vulture in 2013.
"It ran for so long. That's a lot of hours playing one character in front of people. So it's natural that they associate you with that."
More than a decade after the show went off the air, a scene at the end of the show's third season became a GIF. Dawson was watching as his soul mate embarks on a love affair with his best friend and burst into tears.
"It wasn't scripted that I was supposed to cry; it was just one of those things where it's a magical moment and it just happens in the scene," he told Vanity Fair.
He seemed exasperated when he told the Los Angeles Times: "All of a sudden, six years of work was boiled down to one seven-second clip on loop."
Van Der Beek himself recreated the GIF in 2011 for Funny or Die and gave it a second life.
Van Der Beek is survived by his wife, Kimberly, and six children, Olivia, Joshua, Annabel, Emilia, Gwendolyn and Jeremiah.
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