Ashmore is known for playing Marc Hall in Prom Queen: The Marc Hall Story. Since then, he has appeared in the films Safe, A Separate Peace, and A Bear Named Winnie. He has also had guest roles on television shows such as The Eleventh Hour, The West Wing, and 1-800-Missing. Ashmore played the recurring role of Troy Vandegraff on the UPN television series Veronica Mars, as well as the role of Agent Steve Jinks on the Syfy show Warehouse 13.
He was cast as Jimmy Olsen for the sixth season of Smallville on the WB television network and continued to play him into its eighth season. Two years after leaving the show, Ashmore returned to play his character's younger brother on the series finale. Ashmore's twin brother Shawn appeared on Smallville in earlier seasons, and he was offered the role of Jimmy Olsen by director Bryan Singer in Superman Returns before Sam Huntington was cast.
Besides his recurring role on Smallville, Ashmore had roles in the 2007 films Palo Alto, Privileged, The Stone Angel and The Christmas Cottage. He starred in the horror film Fear Island. MTV.ca announced on October 6, 2010, that he would have a role in the Maple Pictures comedy film Servitude.

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