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The museum was dedicated on July 4, 1991 and officially opened to the public on September 28, 1991.The National Civil Rights Museum traces the history of the Civil Rights Movement in the United States from the 17th century to the present. The museum is built around the former Lorraine Motel, where Rev. Martin Luther King, Jr. was assassinated on April 4, 1968. Two other buildings and their adjacent property, also connected with the King assassination, have been acquired as part of the museum complex.

The museum re-opened in 2014 after renovations that increased the number of multi-media and interactive exhibits, including numerous short movies to enhance features. The museum is owned and operated by the Lorraine Civil Rights Museum Foundation, based in Memphis. The Lorraine Motel is owned by the Tennessee State Museum and leased long term to the Foundation to operate as part of the museum complex.

On October 21, 2016, the museum was honored by becoming a Smithsonian Affiliate museum.