The original Duxbury congregation was founded in 1632 by Elder William Brewster as a Christian Separatist church with early members coming from the First Parish Church in Plymouth, the oldest church in New England. In the beginning, the church likely met in congregants' homes until the first meeting house was built near what is today known as Miles Standish Burial Ground. The Duxbury congregation became a parish church of Massachusetts' Congregationalist state church. A schism developed at the turn of the 19th century, when much of the congregation adopted Unitarianism along with many of the other state churches in Massachusetts. State churches were officially disaffiliated with the Massachusetts government in 1834. The current church building was constructed in 1840. The building was added to the National Register of Historic Places in 1978.