The current Capitol is the eighth built to serve as Virginia's statehouse, primarily due to fires during the Colonial period.

The Capitol at Williamsburg served until the American Revolutionary War began, when Governor Thomas Jefferson urged that the capital be relocated to Richmond.

(The others are the Capitols of Alaska, Delaware, Florida, Hawaii, Louisiana, New Mexico, New York, North Dakota, Ohio, Oregon and Tennessee.

The Capitol, the adjacent Virginia Governor's Mansion, and the White House of the Confederacy (about three blocks to the north on East Clay Street) were spared when departing Confederate troops were ordered to burn the city's warehouses and factories, and fires spread out of control in April 1865.

John Brown's carpet-bag, full of documents including many unpublished ones, was kept in the Virginia Capitol from 1860 to 1865 by Andrew Hunter, at that time a state senator.

On July 24, 2020, House Speaker Eileen Filler-Corn ordered the removal of a statue of Confederate General Robert E. Lee, along with busts of J.E.B.

In the ensuing months, a dispute over leadership of the Richmond government resulted in the Virginia Supreme Court of Appeals holding a hearing on April 27, 1870, in the large courtroom on the second floor of the Capitol.

This added weight, in addition to the crowd already there, caused the entire courtroom floor to give way, falling 40 feet (12 m) into the House of Delegates chamber.

Injured included both men contesting the Richmond mayoral position, the speaker of the House of Delegates, a judge and ex-governor Henry H. Wells.

In 1904, two wings (not in the original plans) were added to the east and west ends of the building to provide much-needed additional space for the growing legislature.

These additions were built to the collaborative designs of three of Virginia's leading architects and architectural firms: Frye & Chesterman of Lynchburg, John Kevan Peebles of Norfolk and Noland & Baskervill of Richmond.

The expansion provides a visitor's entrance that is compliant with the Americans with Disabilities Act, plus office space and meeting rooms, and better security management.

It contains several monuments to prominent Virginians and events in Virginia: Given its Classical Revival style of architecture along with the fact that its color is white, the Capitol was the double for the exterior shots of The White House featured in the movie The Contender (2000) starring Gary Oldman, Joan Allen, Jeff Bridges, Christian Slater.