Cockspur Island commands the Savannah River approach to Savannah, a strategic position recognized long before the present fort. British colonial defenses and two earlier United States forts occupied the island, but storms and poor construction defeated those works. After the War of 1812 exposed weaknesses in coastal defense, the federal government adopted a system of large masonry forts. Work on Fort Pulaski began in 1829 under military engineers, including a young Robert E. Lee, and continued until 1847 across marshland that required timber pilings and elaborate drainage.

The completed fort enclosed a broad parade within massive brick walls, casemates, powder magazines, quarters, and a water-filled moat. Millions of bricks came from regional yards, and arches distributed the weight of walls and gun positions across the unstable island. The Army named the fort for Revolutionary War cavalry officer Casimir Pulaski. Although designed to withstand smoothbore cannon fired from beyond their effective range, it saw little active service before South Carolina seceded. Georgia militia seized the nearly ungarrisoned federal installation in January 1861 and Confederate troops strengthened its armament.

Union forces occupied nearby Tybee Island and prepared batteries closer than the fort's designers had thought practical. On 10 April 1862 they opened fire, using experimental rifled cannon whose spinning projectiles struck with greater accuracy and force than traditional smoothbore shot. Within about thirty hours, shells opened a breach in the southeast wall and threatened the main powder magazine. Confederate commander Charles Olmstead surrendered on 11 April. The unexpectedly rapid defeat demonstrated that rifled artillery had made traditional brick coastal fortifications obsolete and allowed Union forces to close Savannah to most Confederate shipping.

The Union repaired the breach and used Fort Pulaski as a prison as well as a base during the remainder of the Civil War. In 1864, hundreds of captured Confederate officers known as the Immortal Six Hundred were confined there under severe conditions. The Army later modernized selected positions with earthen cover and concrete batteries, but the fort lost military importance and was finally abandoned as a defense installation. President Calvin Coolidge proclaimed Fort Pulaski a national monument in 1924, and New Deal workers restored access, drainage, masonry, and visitor facilities during the 1930s.

The National Park Service now preserves the historic brick fort, moat, surviving casemates, parade ground, artillery damage, repaired breach, later batteries, and Cockspur Island landscape. Much of the standing fabric is original nineteenth-century construction, but repointed masonry, reconstructed drawbridge elements, restored rooms, replacement roofs, and modern visitor systems reflect repeated conservation. Trails and exhibits also interpret the island's ecology, labor, imprisonment, and changing military technology. Admission is charged under current park rules, and access can be affected by weather. The site is strongest when read as both an engineered monument and evidence of how quickly engineering assumptions failed.