Jekyll Island lies within the homeland of Indigenous peoples of the Georgia coast and later formed part of Spanish mission, British colonial, plantation, and post-emancipation landscapes. Enslaved Africans and their descendants worked on island plantations before the Civil War, leaving histories that precede the resort district. In 1886 a syndicate of wealthy northern investors purchased the island and organized the Jekyll Island Club as an exclusive winter retreat. The clubhouse opened in 1888, surrounded by service buildings, recreation grounds, docks, roads, and accommodations for employees.

Club members included families associated with banking, railroads, newspapers, oil, manufacturing, and other concentrations of Gilded Age wealth. They hunted, golfed, sailed, bicycled, entertained, and built seasonal residences called cottages, though many were mansion-scale. Architecture ranged from Shingle and Queen Anne designs to Italian Renaissance, Spanish Eclectic, and Gothic Revival forms. Black employees performed essential domestic, grounds, transportation, and service labor within a segregated system, while women workers and family staff sustained the social world presented as effortless leisure. Membership excluded most Americans by design.

The Federal Reserve Act was developed in part through a secret 1910 meeting at the club, adding national financial significance, though the district's history extends beyond that episode. Changing taxes, the Depression, coastal storms, and wartime restrictions weakened the club. It closed during the Second World War. Georgia acquired Jekyll Island in 1947 for a state park and opened the former private preserve to a broader public. New motels, roads, houses, and recreation facilities transformed other parts of the island, while many club buildings deteriorated or found temporary uses.

Preservation accelerated from the late 1960s. The state restored cottages, landscapes, and service buildings, and a public-private project converted the clubhouse into a hotel. The landmark district now contains dozens of historic structures, but they survive at different levels. Some retain extensive original fabric; others have reconstructed porches, renewed interiors, replaced roofs, or adaptive systems. DuBignon Cottage and several service structures were historically moved, and the Skeet House was recently dismantled and reassembled at a new location. Furnishings in toured cottages are curated rather than universally original to each room.

The Jekyll Island Authority manages the state-owned district, while hotel, museum, church, nonprofit, and event uses operate within it. Grounds are generally walkable, and specific tours, museums, transportation, lodging, or programs charge fees. Conservation addresses humidity, termites, salt, storms, accessibility, and large buildings built for seasonal use. The district should not be romanticized simply as Millionaires' Village. Its history connects Indigenous land, slavery, segregation, labor, concentrated wealth, financial power, state acquisition, public recreation, and one of the Southeast's largest continuing programs of restoration and adaptive reuse.