After Twin Peaks went off the air, Ashbrook portrayed Clyde Barrow in the 1992 TV film, Bonnie & Clyde: The True Story alongside Tracey Needham. He starred in the 1995 science fiction TV pilot W.E.I.R.D. World, written and produced by the makers of the Tales from the Crypt TV show. In 1997, he won the starring role of Gary McDermott on the short-lived TV series Crisis Center.
He also starred in the films She's Out of Control (1989), Comfortably Numb (1995), The Last Place On Earth (2002) and Python II (2002). He played the recurring role of Rich Rinaldi on the TV series Dawson's Creek (2002–2003).
Ashbrook has appeared on The WB's Charmed in the 2001 episode "Just Harried", on NBC's The Pretender in the 2000 episode "Rules of Engagement", on The Outer Limits in the 1996 episode "Resurrection", and on Law & Order: Special Victims Unit in the 2007 episode "Haystack".
In 2009, Ashbrook joined the cast of the series Crash for the regular part of Jimmy.
In 2010, he reunited with some of the cast of Twin Peaks on the show Psych. He starred in 2012 in the psycho-thriller The Aggression Scale. Ashbrook is Bobby Briggs in the 2017 revival of Twin Peaks.