The building is a nave-plan, clerestory-style church that includes a corner bell tower and a narthex and chapel in the rear.

[3] In 1881 it was announced that Big Lick would be the location of the junction of the Shenandoah Valley Railroad and the Norfolk and Western Railway (N&W), with both companies moving their headquarters to the small town.

A popular residential area developed south of the city center, and when a lot came available there at the corner of Jefferson Street and Elm Avenue in 1891, a parishioner purchased it for the purpose of moving the church.

[7] This design allowed for a long row of high windows in the church, increasing light and ventilation, while also removing the need for exterior buttressing.

[3] When it opened in 1892, St. John's was the largest church in Roanoke, having been constructed with a seating capacity of 600 though having fewer than 250 members at the time.

[3] An early warden of the church was George Plater Tayloe, a prominent businessman and one of the first trustees of the Valley Union Seminary which became Hollins University.

[3] The congregation's influence in the city was exercised in 1925 when the church was able to defeat a proposal to widen Jefferson Street and force the removal of St. John's altar.

[3] The new office was funded by a grant from Lettie Pate Whitehead Evans, a member of Coca-Cola's board of directors and a prominent Episcopalian from Hot Springs, Virginia.