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In parallel to the activities of French and English settlers in the region and the military operations during the Seven Years’ War (1756-1763), the Jesuits’ actions drew and pushed Kanien’kehá:ka families and other Haudenosaunee communities south of the St. Lawrence River as new alliances were formed. Kanien’kehá:ka peoples had been active in the territory known as Ahkwesáhsne, “the place where the partridge beats its wings,” for millennia prior to the arrival of families from Kahnawà:ke and the Jesuits from New France. The Kanien’kehá:ka families’ and the Jesuits’ presence in the area marked the first permanent settlement in the region, as a new village was erected. The Kanien’kehá:ka and Jesuit presence at Ahkwesáhsne back to 1752, but the Jesuit mission was formally established on June 16, 1755. The first Jesuits who arrived at Akwesasne were initially stationed at Kahnawà:ke through the Saint-François-Xavier Mission. Antoine Gordon, S.J. is considered to be the founder of the St. Regis Mission, and accompanied the Kanien’kehá:ka families when they first arrived in the Ahkwesáhsne region. The Jesuit mission at Ahkwesáhsne was named after Jean-François Régis, S.J., a French missionary who died in 1640 and was canonized in 1737, and who never set foot in North America. Régis had longed to come to North America to convert Kanien’kehá:ka peoples to Catholicism, but his wishes never materialized.

In the aftermath of the Seven Years’ War and the 1763 Treaty of Paris, Jesuits pursued their activities at Ahkwesáhsne, despite the mistrust of the British settlers and First Nations population. The first church seemed to have resembled the longhouses typical of the Haudenosaunee Confederacy. The church, made of wood, was constructed only to burn down in the early 1760s. The fire may have burned the first records of the mission. The church was eventually rebuilt, and, due to the growing community, a stone addition to the church was erected in the early 1790s. Another fire destroyed much of the church in 1866, but it was eventually restored. Several additions and changes were made, but the church—still standing in the early 21st century—includes the original early-1790s foundation.

From 1752 to 1783, the Jesuits managed the St. Regis Mission. Mostly secular priests then replaced the Jesuits until 1937, when the Jesuits priests overtook the mission once again.