This congregation was founded in the 1650s, not long after Puritan settlers came to Southampton. It was officially organized in 1741. The current church building was originally located in the Hampton Bays. It was dragged across the Shinnecock Bay by horses during the 1800s and moved to the Shinnecock Indian Reservation. The building was moved and turned by the Great Hurricane of 1938, and instead of moving or replacing the church, an extension was added on. The extension became the space for worship, and the original part of the building is now the parish hall. The church office is next door.
Services take place at 10 a.m. on Sundays in the summer and at 11 a.m. in the winter. There is Holy Communion on the first Sunday of the month. On the third Monday of the month, Shinnecock Presbyterian serves a free community dinner at 6 p.m. On Tuesdays, there is Bible study and beading. The choir practices Saturday at noon. The church puts on a homecoming on the first Sunday in June for Shinnecocks who live elsewhere to visit the reservation.
Half the proceeds of the Shinnecock Indian Nation's annual powwow go toward supporting the church.
The church participates in SAMP, Substance Abuse Mobilization Project, a faith-based health program.
The Reverend Mike Smith has been pastor since 1985.
