In 1852, the Orange and Alexandria Railroad built two depots at this location, one on the east side of the tracks for freight and one on the west side of the tracks for passengers. Although these buildings survived the Civil War, including the Battle of Culpeper Courthouse on September 13, 1863, the occupation and fighting took their toll.
In 1874, a new Culpeper town depot was built, which later burned in 1903. A year later, the present building was completed to replace it. Years of use and subsequent decline led Norfolk and Southern Railroad to request permission in 1985 to demolish a portion of the Depot.
A committee formed to save and renovate the building, a project that was completed in 2003. Today, the beautifully restored Depot houses the Visitor's Center, the Chamber of Commerce, the Department of Tourism, and space for meetings and conferences.