In 1684, the Newport Quaker Monthly Meeting recognized the growing Quaker community in Jamestown and established the Conanicut Friends Meeting which met at the home of Nicholas Carr. The founders raised the first meetinghouse on North Ferry Road in 1709-1710 where the Friends Burial Ground is today. In 1734 they moved the building to the current site at the corner of North Road and Weeden Lane where it remained through the Revolutionary War.

The meetinghouse was the only house of worship on the island for 150 years. It was the spiritual center of the community, and most residents of European ancestry were Quakers. There is no record of the over 100 enslaved or free African American and Indigenous people being included in any meetinghouse activities. After the Friends Rhode Island Yearly Meeting of 1773 decided slaves ought to be freed, some freed their slaves outright or converted them to indentured servitude, while others sold them.

During the Revolutionary War, the Friends Meeting records reveal that most Quakers left the island, abandoning the building. British soldiers then occupied it and the meetinghouse “suffered considerably from them”. In 1786 the congregation built a replacement at the same time the windmill was constructed. It is a simple shingled rectangular building and is still in use today for worship services in the summer.

At the beginning of the 19th century, the Quaker community in Jamestown became too small to sustain the meeting and the building fell into disuse. The meetinghouse was reopened in the early 1900s for summering Philadelphia Quakers. The size of the Conanicut Meeting has waxed and waned over the years, but has grown since 2020. The Jamestown Quaker community continues to preserve the spirit of Quakerism in silent worship in that simple place.

The National Register of Historic Places added the meetinghouse to its roster in 1972, and in 1976-1977, with matching funds from the Rhode Island Historical Preservation & Heritage Commission, the Conanicut Meeting repaired the building. Further restoration was completed in 1997 with a grant from the Champlin Foundation. In September of that year, title to the meetinghouse was transferred to the JHS, with the provision that the building would be open to the Conanicut Meeting for worship during the summers.