In 1814, St. John's Episcopal Church was organized and first met in the Ontario County, New York Court House in Canandaigua.

It contains several windows from the earlier wooden church, elaborate new stained glass windows imported from Europe, and one—The Parables Window—was designed by Daniel Cottier, who was considered an important influence on Louis Comfort Tiffany.

In 1964-1965, an addition to parish house included classrooms, a new chapel, and a dining/ meeting room added to celebrate the church's 150th anniversary.

Recent additions include a columbarium with a capacity of 136 niches and a memorial garden, outside the church.

A capital campaign begun in 2017 allowed the parish to upgrade and improve five areas identified by parishioners as essential priorities.

Joseph Wayland, Rector 1850 — Trinity Church, Wall Street (NYC) gifts St John's $1,500.

1867 — Church enlarged with 26 additional pews, repaired, painted, stoves removed and furnace added.

St. John's is built of various kinds of stone and its intricate and colorful display of stained glass windows is one of the most impressive in this area.

1880 — Bell installed as memorial to Moses Atwater, first Warden, by descendants 1886 — May 6, church consecrated after payment of debt.

1895 — Permanent endowment fund established with legacy of $1,000, "interest only to be applied to current expense of the church."

Eugene Marsden Chapman, Rector 1940 — Chapel established in south transept of church in memory of Frances Paul.

Columbarium and chapel dedicated and blessed by the Right Reverend Prince Grenville Singh, Ph.D., Bishop of Rochester.

David Hefling, AOJN+, Rector 2011 — Complete redesign/restructuring of the parish hall to expand space and use as a reception area.

Gardening program is launched as is "Red Wagon Food Pantry" - both to benefit Gleaners Kitchen.

Joanne Wisor, a parishioner at Trinity Church, Geneva, NY, is appointed as Assistant Archivist.

2018 — The Reverend Patti Blaine, Deacon, is assigned to the parish by Bishop Singh.