The restoration of the interior of the original 18th-century building, now the transept began in the early 1970s. The work was sponsored by the St. John's Church Foundation, which was established in 1938 to preserve and maintain the church as an historic monument. In the 1960s, during work to repair a leak in the roof, it was discovered that the church's structure was in need of serious restoration. A national appeal was begun to pay for the needed work and endow a fund to be used for future restoration projects. The State of Virginia appropriated $100,000 in 1966 toward the $250,000 that was raised by 1971. Mr. Vernon Perdue Davis and Mr. J. Scott Rawlings guided the Foundation throughout the project with their careful research. The reconstructed interior portrays as accurately as possible an Anglican Church in Virginia during the 18th century. The work on the interior continues to be refined to this day.
Little of the original interior remained. Most notable was the survival of the sounding board, pews, and wainscoting. It was possible to use much of the original wood in the newly restored tall pews. The dignitary's pew, the clerk's pew and the pulpit are composed almost entirely of original paneling and wainscoting. The reconstructed tall pews on either side of the transept were made to complement the originals.
The colonial chancel was designed through careful study of remaining 18th century Anglican churches in Virginia and Maryland. A 19th century door on the east wall was removed before beginning work on the altar. Canon law and tradition dictate that the east wall was always the site of the altar. The stunning catechetical tablets were fashioned after the surviving example from Aquia Church, Stafford County, Virginia and from a photograph taken by Matthew Brady during the Civil War of the now destroyed Falls Church in Fairfax County. The lettering was derived from a tablet surviving at Christ Church, Alexandria. Canon law required the Decalogue and various injunctions (royal and Episcopal), the Belief, the Lord's Prayer, and Scripture Sentences must all appear on the catechetical tablets. On either side of the altar are reconstructed windows, copied from the original ones that survived in the church. The holy table was made in England, partly designed from an example surviving near Salisbury, Maryland. The needlepoint kneelers, though not colonial in design, represent the original thirteen colonies. They were made by a group of dedicated women from Virginia and Washington, D.C.