Though the town of Falmouth, Massachusetts, was incorporated in 1686, the town did not have a formal congregational church until over 20 years later. The town's inhabitants largely belonged to the Congregational Church in Barnstable and worshiped in Falmouth at a "branch church." The first minister of the Falmouth community was, Jonathan Dunham, a lay preacher, who served from about 1677 to 1684. He was followed by another lay preacher, Samuel Shiverick, a Huguenot refugee, who served from about 1687 to 1703. The first meeting house was probably built between 1690 and 1700. In 1707 Josiah Metcalf was called to serve as the minister. On October, 10, 1708, the First Congregational Church in Falmouth, was formally gathered and Josiah Metcalf was ordained as the church's first minister. He served as the minister until his death in 1723. In 1717 the second meeting house was constructed to replace the first. Construction on the third meeting house, known as the meeting house on the green, was completed in 1750 after eight years of discussion during church meetings.
A church library was established in 1789. By 1791 the church building was in disrepair; the fourth, and final, meeting house constructed to replace the 1750 building, was completed in 1796. The church purchased a bell from Paul Revere for the new building; the bell is still housed at the church today. In 1821, 77 members withdrew over theological differences with Rev. Henry Lincoln and his adoption of a particularly strict Confession of Faith. They formed the East End Church in Hatchville. Even after Rev. Lincoln was forced to resign in 1823, the church continued to lose members over his theological beliefs, with many being dismissed to the Methodist Episcopal Church in Falmouth. In 1824 the church established a Sunday school. In 1833, nine members withdrew to form the North Falmouth Congregational Church; it appears that these members disagreed with the church's adoption of a strict temperance resolution. In 1837 the first church missionary society was founded. In 1857 the meeting house was deconstructed and rebuilt, with significant changes done to the steeple, windows, and pews, on its present location.
The First Congregational Church in Falmouth continues to serve the local community and is now a member of the United Church of Christ.