The Mississippi Room, 1906, when the collections were displayed in the White House of the Confederacy.Visitors to the Confederate Museum encountered a building and a collection that changed little from the 1890s through the 1950s. About 7,000 people a year visited the Museum in the era before World War I. That number grew to over 10,000 per year in the 1920s through the 1940s, and to 20,000 by the mid-1950s. Upon coming to the mansion's entrance hall, visitors were greeted by a doorman and a guide. The guide collected 25 cents admission fee, fetched change, and asked visitors to sign the guest register. Visitors were then led into the Solid South Room, where the house regent kept her desk. Beginning with the Virginia Room the largest in the building visitors wove their way in and out of spacious, high-ceilinged rooms filled with free standing ebony and glass cases and document stands, and walls covered with portraits.

However, even sympathetic visitors could not help but notice the problems of the Confederate Museum. "Dust-proof" and "moth-proof" cases were ineffective against insects, strong sunlight, and humidity. The monthly "freshenings" and annual spring cleanings by the vice regents could not keep away the dust or cobwebs. Citizens were beginning to refuse donations because of the lack of protection that was provided for the collections of the Museum.

By 1960, Society members recognized that the Museum had reached a crossroads. The celebrations of the Civil War Centennial brought the Museum renewed attention and highlighted its problems mainly space. The Museum was described as "badly overcrowded." By that time, the Society had committed the Museum to new vision incorporating professionalism and change. The Museum’s preservation practices would be updated to meet modern standards. Additionally, they would consider moving the military collection and library out of the White House and restoring and furnishing that building as the residence of Jefferson Davis.

Immediately, the Museum adopted policies to project the image of a modern institution dedicated to using its renowned collections to advance the study and understanding the Confederacy and the American Civil War. For that reason, the Museum's name changed from the Confederate Museum to The Museum of the Confederacy. The first professional staff was hired to implement new practices and manage the organization. With the assistance of a prestigious group of national trustees, the Society raised funds to build a new Museum facility and restore the White House to its wartime appearance by marketing Lenox plates with such designs as the White House and scenes from the Museum’s collection of Conrad Wise Chapman and William Ludwell Sheppard artworks.

The dedication of the completed modern museum building was held in October 1976. Between 1976 and 1978, the collections were transferred out of the Davis mansion. The White House was closed for the next ten years for the overwhelming task of restoring its environs to a wartime state. The staff, along with consultants and specialists, examined the building and all available documentary sources for clues about the appearance of the rooms and the events that occurred within them. Original White House furnishings (many of them in the collections since the 1890s) were repaired and upholstered in reproduction fabrics based on surviving samples of White House originals. Davis family personal possessions and other appropriate period furnishings complemented the display. In June 1988, the meticulously restored White House opened to the public.