St. John's is located in the center of the Warehouse Point village, just south of the junction of Main and Bridge Streets. It is a tall single-story wood-frame structure, with a projecting entry section, and a two-stage square tower housing a clock and bell. The main block's corners are pilastered, as are those of the projection, and there are full-height pilasters flanking the main entrance, above which is a stained-glass Palladian window.[2]
The interior is a distinct contrast to the building's exterior. As originally built, it had a fairly traditional 18th-century meetinghouse plan, with a flat ceiling, galleries on the sides, and a Palladian window behind the pulpit. In 1855, the congregation retained the New Haven firm of Henry Austin to redesign it in the Gothic style. The side galleries were removed and the ceiling was transformed into a barrel vault, with a new chancel at the rear.[2]
The church was designed by Samuel Belcher and built in 1809, and originally stood on the village green. It served as a union church serving both Methodists and Episcopalians until 1832, when the Methodists built their own church.[3] It was moved to its present location in 1844.[2]