In 1861, the Civil War began. Florida joined the Confederacy, but Union troops loyal to the United States Government quickly occupied St. Augustine and remained in control of the city throughout the four-year long war. Twenty years after the end of that bitter conflict, St. Augustine entered its most glittering era.

Henry Flagler, a former partner of John D. Rockefeller in the Standard Oil Company, decided to create in St. Augustine a winter resort for wealthy Americans. He owned a railroad company that in 1886 linked St. Augustine by rail with the populous cities of the east coast. In 1887, his company began construction of two large and ornate hotels and a year later added a third that had been planned and begun by another developer. Flagler's architects changed the appearance of St. Augustine, fashioning building styles that in time came to characterize the look of cities throughout Florida. For a time, St. Augustine was the winter tourist mecca of the United States.

In the early twentieth century, however, the very rich found other parts of Florida to which they could escape. With them fled Flagler's dream of turning St. Augustine into the "Newport of the South." St. Augustine nevertheless remained a tourist town. As Americans took to the highways in search of a vacation land, St. Augustine became a destination for automobile-borne visitors. The tourism industry came to dominate the local economy.

The city celebrated its 400th anniversary in 1965 and undertook in cooperation with the State of Florida a program to restore parts of the colonial city. In 1997 the City took over full responsibility for what locally had become known as the "Restoration" and with it management of the more than thirty-six buildings that had been reconstructed or restored to their historic appearance.