The name honored Thomas Fairfax, 6th Lord Fairfax of Cameron (1693–1781)[7] who was proprietor of the Northern Neck peninsula, a vast domain north of the Rappahannock River; his territory was then defined as stretching from Chesapeake Bay to what is now Hampshire County, West Virginia.

The original plan of the town called for ten blocks, which form the core of Culpeper's downtown area today.

During the Civil War (1861-1865), Culpeper was a crossroads for a number of armies marching through central Virginia, with both Union and Confederate forces occupying the town by turn.

One block north on Main Street (present location of Piedmont Realty) was the frame house where "The Gallant Major" John Pelham died after sustaining a wound at the Battle of Kelly's Ford.

[8] Culpeper began to grow dramatically in the 1980s, becoming a "bedroom community" of more densely populated Northern Virginia and Washington, D.C. suburbs.

In 2011, East Davis Street in downtown Culpeper was named as a 2011 America's Great Place by the American Planning Association.

[10] The earthquake led to the temporary evacuation of the Packard Campus for Audio-Visual Conservation, which at the time was hosting a town hall event for U.S.

As of the 2010 census, the racial makeup of the town was 61.5% White, 21.9% Black, 0.6% Native American, 2.1% Asian, 0.01% Pacific Islander, and 4.0% from two or more races.

[citation needed] Culpeper houses many local restaurants, shops and stores in its historic downtown.

[16]  In recent years many improvements have been added to provide new activities and opportunities to the community such as the reopening of The Dominion Skate Park and State Climb.

Nearly 9,000 train passengers in 2010 used Culpeper station, which connects to New Orleans, Chicago, Cincinnati, New York and Boston via the Crescent, Cardinal, and Northeast Regional lines.