Television and film
In early 1997, Van Der Beek auditioned for three television pilots, including one for the WB series Dawson's Creek. He was cast as the title role of Dawson Leery, and the show's 1998 premiere became a breakout success that helped establish the network and its cast. The series ran for six seasons and was syndicated worldwide. In 1999, he starred in the teen football drama Varsity Blues, which held the number-one spot at the U.S. box office for its first two weeks, and he won an MTV Movie Award for Best Male Breakthrough Performance.
Around this time, Van Ber Beek was named one of People magazine's "50 Most Beautiful People in the World", and he appeared in several films, including Texas Rangers, Scary Movie and Jay and Silent Bob Strike Back, in which he played himself playing Jay opposite Jason Biggs as Silent Bob. In 2002, he portrayed Sean Bateman, younger brother of American Psycho protagonist Patrick Bateman (Casper Van Dien), in Roger Avary's film adaptation of Bret Easton Ellis' The Rules of Attraction. The film was a box‑office disappointment but later developed a cult following on DVD.
In 2006, Van Der Beek appeared in the direct-to-DVD thriller The Plague, produced by Clive Barker, which was panned by critics. After Dawson's Creek ended in 2003, he returned to Off-Broadway in Lanford Wilson's Rain Dance. He completed an unproduced screenplay titled Winning and made several television appearances, including a role on Ugly Betty. In 2007, he guest-starred in a two-part episode of Criminal Minds, playing serial killer Tobias Hankel, who kidnaps and drugs Spencer Reid (Matthew Gray Gubler). In 2008, he appeared on How I Met Your Mother as Simon Tremblay, one of Robin Scherbatsky (Cobie Smulders)'s former boyfriends, returning for two more episodes in 2013.
In 2008, Van Der Beek began a recurring role on One Tree Hill as Adam Reese, a filmmaker who served as a satirical opposite of Dawson Leery. He appeared in an episode of the fifth season of Medium. In 2009, he portrayed real‑life kidnapper Anthony Steven "Tony Zappa" Wright in the Lifetime film Taken in Broad Daylight. Also in 2009, he won Best Actor at the 8th Annual San Diego Film Festival for his performance as FBI agent Jake Kelly in the political thriller Formosa Betrayed, which also won Best Picture. The film received a U.S. theatrical release on February 26, 2010. On January 5, 2010, TV Guide reported that Van Der Beek had been cast in a major recurring role on the NBC medical drama Mercy, playing Dr. Joe Briggs, the new womanizing ICU chief with a dark secret. He also appeared in the thriller Stolen, starring Rhona Mitra, Josh Lucas and Jon Hamm. In 2011, Van Der Beek played Kesha's nemesis in her music video for "Blow". He then portrayed a fictionalized version of himself on the ABC sitcom Don't Trust the B— in Apartment 23. The show debuted to critical praise, with Van Der Beek receiving acclaim for his comic timing and self‑parody.
From 2015 to 2016, Van Der Beek played the role as Senior Field Agent Elijah Mundo on CSI: Cyber. In 2017, he appeared in the British comedy series Carters Get Rich. He made a cameo in the film Downsizing (2017), starring Matt Damon, and voiced Boris Hauntley in the Disney Junior series Vampirina. Van Der Beek co‑created, wrote, produced, and starred in What Would Diplo Do?, portraying producer and DJ Diplo. He was also a showrunner for the series. The show premiered on Viceland to positive reviews both for the writing and his performance, was described, "The Veep of DJ Culture" by the Los Angeles Times and received a 90% rating on Rotten Tomatoes. In 2019, Van Der Beek was cast as Matt Bromley on the FX drama Pose, a role he played for one season.
He joined the cast of the 28th season of Dancing with the Stars, partnered with professional dancer Emma Slater. A strong performer, he consistently placed near the top of the leaderboard and was widely considered a frontrunner until his elimination in the semifinals, finishing in fifth place. That night, he revealed that his wife, Kimberly Brook, had suffered a miscarriage two days earlier. His elimination, following the judges' lowest score of the night, was controversial among fans.
In 2025, Van Der Beek competed on season thirteen of The Masked Singer as "Griffin", whose costume featured wings that opened during performances. Clues referenced his illness. He was eliminated in the "Group B Finals: Grand Ole Opry Night," and host Nick Cannon surprised him by bringing his wife Brook and their children onstage. In 2026, he posthumously appeared in John Burr's feature film The Gates by Lionsgate Premiere, and the Legally Blonde prequel television series Elle.