St. John's is the oldest church in the city of Richmond. It was built in 1741 by Colonel Richard Randolph, and the Church Hill neighborhood was named for it. It stands at 2401 East Broad Street and is a National Historic Landmark.
The church was the site of two important conventions in the years before the American Revolution. It is famous as the place where Founding Father Patrick Henry gave his speech at the Second Virginia Convention.
The parish grew out of earlier ones. The first, Henrico Parish Church, was at Henricus in 1611. Henricus was destroyed in 1622 and was never rebuilt.