It was founded in 1886 when members of an incorporated hunting and recreational club purchased the island for $125,000 (about $3.1 million in 2017) from John Eugene du Bignon.

The club thrived through the early 20th century; its members came from many of the world's wealthiest families, most notably the Morgans, Rockefellers, and Vanderbilts.

In 1947, after five years of funding a staff to keep up the lawn and cottages, the island was purchased from the club's remaining members for $675,000 (about $7.4 million in 2017) during condemnation proceedings by the state of Georgia.

In 1885, Finney and a New York associate, Oliver K. King, gathered a group of men and petitioned the Glynn county courts, becoming incorporated as the "Jekyl Island Club" on December 9, 1885.

Six of the first seven shares went to the men who signed the charter petition: Finney, du Bignon, King, Richard L. Ogden, William B.

In all, Finney was able to find 53 people to join the club, including such famous names as Henry Hyde, Marshall Field, John Pierpont Morgan, Joseph Pulitzer, and William K.

These men faced the difficult task of turning the undeveloped property into a social club for the wealthy upper class of America.

Several nationally important events took place on Jekyll Island during the Club era, including the first transcontinental telephone call made by Theodore N. Vail, president of AT&T, to Alexander Graham Bell, Thomas A. Watson and President Woodrow Wilson in 1915; and the development of the Aldrich–Vreeland Act for the National Monetary Commission in 1908.

[6] Jekyll Island was the location of a meeting in November 1910 in which draft legislation was written to create a central banking system for the United States.

Senator Nelson Aldrich (R-RI), chairman of the National Monetary Commission, went to Europe for almost two years to study that continent's banking systems.

Upon his return, he brought together many of the country's leading financiers to Jekyll Island to discuss monetary policy and the banking system, drafting legislation which was introduced in Congress as the "Aldrich Plan".

Andrews (Assistant Secretary of the United States Treasury Department), Paul Warburg (a naturalized German representing Kuhn, Loeb & Co.), Frank A. Vanderlip (president of the National City Bank of New York), Henry P. Davison (senior partner of J. P. Morgan Company), Charles D. Norton (president of the Morgan-dominated First National Bank of New York), and Benjamin Strong (representing J. P. Morgan), together representing about one quarter of the world's wealth at the time, left Hoboken, New Jersey on a train in complete secrecy, dropping their last names in favor of first names, or code names, so no one would discover who they all were.

Forbes magazine founder Bertie Charles Forbes wrote several years later: Picture a party of the nation's greatest bankers stealing out of New York on a private railroad car under cover of darkness, stealthily riding hundreds of miles South, embarking on a mysterious launch, sneaking onto an island deserted by all but a few servants, living there a full week under such rigid secrecy that the names of not one of them was once mentioned, lest the servants learn the identity and disclose to the world this strangest, most secret expedition in the history of American finance.

Senator Aldrich notified each one to go quietly into a private car of which the railroad had received orders to draw up on an unfrequented platform.

During the financially difficult Great Depression period, the club began referring to its members as founders and created the new Associate Membership.

It contains thirty-three contributing properties from the Jekyll Island Club, including the separately-NRHP-listed Rockefeller Cottage and Faith Chapel.

From 1967 to 1968, Savannah landscape architect Clermont Huger Lee created a master development plan with the goal to restore the area known as "Millionaire's Village" to its 1910–1929 era.

Though not fully implemented, Lee's plans served as a foundation in the redevelopment of today's Jekyll Island Historic District.