The gap serves as the western demarcation point for the border between Fauquier and Loudoun counties, originally marked by a "double-bodied poplar tree standing in or near the middle of the thoroughfare of Ashby's Gap on the top of the Blue Ridge.

"[2] The tree has since died[2] and the thoroughfare, modern day U.S. Route 50, realigned to the south so that Loudoun County is not entered when traveling through the gap.

Upon European colonization, the gap was first referred to as the "Upper Thoroughfare of the Blue Ridge".

Stuart's cavalry held this gap to prevent elements from the Union Army under Major General Joseph Hooker from interfering with General Robert E. Lee's army as it marched north toward Pennsylvania in the Gettysburg Campaign.

[citation needed] On July 19, 1864, a small cavalry battle, sometimes referred to as the Battle of Ashby's Gap, was fought at the gap when Union cavalry attempted to force passage across the gap and Shenandoah River in an attempt to attack the rear of Confederate Lieutenant General Jubal Early's army and supply trains as he repositioned himself near Berryville as part of the Valley Campaigns of 1864.