The history of the museum dates back to 1965 when the "Red River Art Center" opened in the former Moorhead, Minnesota, post office. The name of the museum was changed when it was incorporated with the Rourke Art Gallery to form the "Plains Art Museum" in 1975. After a 1987 schism resulting the departure of founding director James O'Rourke, the Plains Art Museum and the Rourke Art Museum and Gallery became separate institutions. The Museum remained in the downtown Moorhead location until 1996. In October 1997, the Museum relocated to a renovated turn-of-the-century International Harvester warehouse in downtown Fargo, North Dakota. The American Alliance of Museums granted accreditation to Plains Art Museum in 2003.  This made the Plains Art Museum one of two museums in North Dakota which has received this distinction. 
The Plains Art Museum acquired the old International Harvester warehouse building in 1994.
The museum's permanent collection contains approximately three thousand works including national and regional contemporary art, traditional American Indian art, and traditional folk art. Artists whose work is represented include Andy Warhol, James Rosenquist, Salvador Dalí, Ellsworth Kelly, Helen Frankenthaler, and Sol LeWitt. 
In 1993, the Plains Art Museum began the Rolling Plains Art Gallery, a climate-controlled semi-trailer which traveled to communities in North Dakota and Minnesota. The semi-trailer not only transported the artwork, but also served as the gallery itself. To create a richer experience, an art educator travelled along with the select pieces from the permanent collection.  The Rolling Plains Art Gallery is not currently touring.
- "Plains Art Museum - Museum Facts & History". plainsart.org. Archived from the original on 2007-05-11.
- Jessica R. Anderson, Arts & Entertainment editor (8 May 2007). "Plains Art Museum offers great fun". The Spectrum. Archived from the original on 4 July 2007.CS1 maint: Extra text: authors list ( link)
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