Van Der Beek seemed increasingly uncomfortable during the exchange, commenting negatively on a picture from the show on the TV behind the presenters.
His curt answers included admitting he'd never watched all of the show he's most well known for.
The 40-year-old hunk rocketed to fame in 1998 thanks to his portrayal of Dawson Leery in the US teen drama but confessed he has only seen some episodes from the seven series of the hit show.
Asked whether he had watched all of it, Van Der Beek confessed: "No, actually I didn't. At a certain point it became easier to do it and to kind of let it go".
Viewers quickly noted the awkward exchange.
Despite going on to star in the likes of Ugly Betty and Criminal Minds, Van Der Beek remains best known for his breakthrough role.
Later, Van Der Beek said he didn't mind being remembered for playing Dawson because it changed his life.
He said: "It was a huge opportunity, I learned how to be in front of a camera, I learned how to be a celebrity I learned how to deal with all kinds of things- it was a huge big break. I wouldn't change anything."
The actor will be seen next playing a fictional version of the real DJ Diplo in a new TV series for Viceland called What Would Diplo Do? and has finished filming Sky1's Carter's Get Rich, in which James plays a billionaire who changes the lives of a working class British family.
Speaking about the role, he said: "It's about a boy from Milton Keynes who develops a dating app - a really obnoxious American billionaire - which is me. The most fun characters to play are kind of the ones who drive the scenes and disrupt things."
- Bang! Showbiz
