During the mid-1860s, Major General John Pope had put forth plans to create a line of forts across the newly formed Dakota Territory.

Although Pope canceled his plans for this fort in the fall of 1864, efforts to establish a military foothold there were revitalized in early 1867.

[3] By 1868, soldiers—United States Army infantrymen who were garrisoned there—were already constructing more permanent buildings, although official authorization from Congress to do this was not granted until April 6, 1869.

Most were built from bricks crafted from locally sourced clay and lime quarried at Devils Lake and placed on stone foundations.

[citation needed] As war waned and the threat of raids dwindled, the army struggled to justify its upkeep of a strong military presence across the American frontier.

With the army unable to justify its presence on Devils Lake any longer, Fort Totten was decommissioned and abandoned on December 20, 1890.

[3] After its decommissioning, Congress turned over Fort Totten to the Bureau of Indian Affairs, who repurposed it into a Native American boarding school.

[6] Most pupils were from western North Dakota and Montana; most local families, especially those at Spirit Lake, favored St. Michael's Mission due to Fort Totten's rigid structure and English-only curriculum.

By 1910, Fort Totten had introduced a system that allowed local students to commute and live at home, rather than boarding.

[7] Its financial situation never recovered after the Great Depression, and in 1959, a new campus opened east of the Fort Totten location.

On March 6, 1959,[3] Fort Totten ceased operations and the BIA turned the property over to the State Historical Society of North Dakota; its ownership began in 1960.

[2] One of the former officers' quarters was restored and converted into the Totten Trail Historic Inn in 2001 and 2002, which functions both as a hotel and also as a conference and event venue.