Ferrisburgh Monthly Meeting was established as a monthly meeting in 1801 by Easton Quarterly Meeting. In 1804, the Quarterly Meeting discontinued the monthly meeting at Ferrisburgh and replaced it with a monthly meeting to be held at Monkton. Eleven years later, in 1815, Monkton Monthly Meeting was divided into two monthly meetings, one to be called Ferrisburgh, including the members of the preparative meetings at Monkton and Ferrisburgh, and one to be named Starksborough, including the members of Starksborough, Lincoln, and Montpelier. Ferrisburgh Monthly Meeting was further divided into Hicksite and Orthodox branches after the Separation of 1828. Ferrisburgh Monthly Meeting (Hicksite) was laid down in 1846 and members were joined to Peru Monthly Meeting. Ferrisburgh Monthly Meeting (Orthodox) circulated between the meeting houses at (North) Ferrisburgh, Charlotte, Monkton Ridge, and South Starksboro (also called Creek) in the late 19th century.

Levinus K. Painter assumed the position of pastor of the three small meetings in Ferrisburgh Quarter in 1921; by that time, the meeting at North Ferrisburgh had become inactive, but there were meetings at Monkton Ridge and South Starksboro. In 1925, Ferrisburgh Monthly Meeting of Friends requested permission from Ferrisburgh Quarterly Meeting to establish a class of membership known as "Affiliated;" this was to accommodate the members of two Methodist churches in Monkton Ridge who had associated with Friends to meet together in the meeting house at Monkton; they eventually formed a single congregation, known as the Monkton Church at Monkton Ridge and as Friends Methodist Church. The name of Ferrisburgh Monthly Meeting was apparently changed after 1925 to Monkton Monthly Meeting. The latter was finally laid down in 1996 by Northeastern Regional Meeting.