The museum opened in 1935 with art borrowed from other museums. The first work in the Murdock Collection was purchased in 1939. Mrs. Murdock’s friend, Elizabeth Stubblefield Navas, selected and purchased works of American art for the Murdock Collection until 1962. The building was enlarged with a new lobby and two new wings in 1963. In 1964, a foundation was established for the purpose of raising funds for new acquisitions. In the 1970s, the city built a new and larger climate controlled facility. In 2003, the museum finished another expansion project giving the building 115,000 total square feet.