On June 17, 1869, a meeting was held in "The School House, District No. 3, Town of Smithtown," for the purpose of electing the first Board of Trustees for the church. The Rev. D.F. Hallock, appointed by the Methodist Conference to serve St. James and Stony Brook, became the first pastor of the St. James Methodist Church....called at that time "The Thompson Methodist Episcopal Church of St. James." On June 27, 1870, a parcel of land of slightly more than five acres was conveyed by Gideon and Sarah Smith to the church. The first building was erected in 1872-1873 on the site of the present church. It was a small, white, wooden structure, measuring about 20 feet by 40 feet. Standing on the crest of a hill overlooking thickly wooded terrain, it became known as "The Church on the Hill" and for twenty-four years served as an inspiration for all who attended.

Then on the night of October 13, 1897, the church was completely destroyed by fire. Less than two months after the fire, work on a new church began. A design was chosen, a building committee was appointed and a contract signed to begin immediate construction. The cornerstone was laid on March 14, 1898, and on June 5, 1898, the newly built church was dedicated. It was completed at a cost of $2,400, including furnishings. This church building is the present church sanctuary with the exception of a few minor interior alterations. It has served the community for over 100 years, in good times and bad, and always with unselfish devotion and sacrifices on the part of the pastors and the church members.