A long-ago $500 gift from Trinity to the new parish on Long Island helped clear the debt left by the congregation of Episcopalians who worshiped in a little red schoolhouse near the present church during the first thirty years of the 1800s.

Smith Sammis was chosen as architect-builder of the new church and construction took place in 1835 at a cost of $3,215. Limon Rice, whose name was sixteenth on the Vestry Minutes list of contributors as having given $1, was the first sexton. The first Vestry list names William and John Jones ($200 contributors each to the building fund) as wardens, William, John, Walter, Joshua and David Jones, John and Jacob Hewlett (who married Jones girls), Samuel Youngs and Richard Conklin as vestrymen. The Rev. Benjamin Treadwell Onderdonk, Bishop of the Diocese of New York, consecrated the building on April 5, 1837.

The Vestry called the Rev. Isaac Sherwood as first Rector. Little is known about the man, but he must have been beloved: His name is on the founders' window, now hidden behind the curtain above the altar, and he is one of the few non-family members buried in the family burial ground on the hill west of the church.

Although its influence waned slowly as the congregation grew and diversified, the Jones family remained St. John's first family. More land was given as the church needed to expand, and land for St. John's Memorial Cemetery a mile to the west was deeded to the church in 1862. Two generations later when the congregation could not afford the Jones's generous offer to sell them the pond for $25,000 in the 1930s, the Jones family put up $20,000 of the asking price and the congregation was able to raise the rest.