The museum is located in the former administration building of the Auburn Automobile Company, which operated on this property from the early 20th century until its closure in 1937.

[2][3] The showroom and administrative buildings were designed by architect Alvin M. Strauss in Art Deco style and were built in 1930.

After its closure, the administration building housed a business selling original and reproduction parts for a number of discontinued manufacturers, including the Auburn, Cord, and Duesenberg nameplates, until 1960.

[3] The museum is organized into seven galleries that display over 120 cars and related exhibits such as restored Auburn Automobile company offices.

Some exhibits have interactive kiosks that allow a visitor to hear the sounds the car makes and to see related videos and photographs that show the engineering that went into its design.