The Totten Trail Historic Inn building has a rich history. Uses of the building were as Officers' Quarters during the military period (1867 - 1890) and as a residence hall during the Indian Industrial School period (1891-1935). The building was constructed by the United States Government in 1869 to serve as quarters for four officers and their families who were stationed at Fort Totten Military Post. Each officer had a separate apartment from the other officers' families in this quadraplex structure.

In 1890 the military decommissioned the post, and the site was converted for use as in industrial school for children from the Devils Lake Sioux Indian Reservation (now known as Spirit Lake Dakota Nation) and Turtle Mountain Band of Chippewa Tribes. The building was used as apartments for the school employees. Wains coating was added to the walls. The entire structure came to resemble a grand hotel of the period. The Inn has retained the school era floor plan. Special features retained from the school era are a grand staircase in the entrance, and original stamped-tin covered kitchen walls, and a large parlor area that was used as a dining hall by the school era employees.

With the receipt of an ISTEA grant and matching funds raised through the spearheading efforts of the Fort Totten State Historic Site Foundation, individuals, groups, businesses, and other supporters of Fort Totten State Historic Site the restoration and modern adaptive use project on the building began in 1997.

William Latoza of BauerLatoza Studio, Chicago, Illinois, and Peter Miejer of Sera Architects, Portland, Oregon performed the necessary architectural work for renovation of the building. The general contractor was Robert Mackley Associates of Minot. Lake Region and state subcontractors were also used.