The caverns may have been familiar to Native Americans since long before their discovery by Europeans, though there has been no documented evidence of human presence in the cave before the late 1800s. The Lewis and Clark Expedition camped within sight of the caverns on July 31, 1805, when they camped along Antelope Creek. In 1892, local ranchers Tom Williams and Bert (or Burt) Pannel saw steam coming from the caverns while hunting. Following the discovery, two people from Whitehall, Montana, Charles Brooke and Mexican John claimed that they had discovered the cavern in 1882. However, their claims are unsubstantiated. In 1898, Williams finally explored the caverns with some friends.

The cave was first developed for tours around 1900 by Dan A. Morrison, who called it Limespur Cave. He filed a mineral claim on the land in 1905, but the Northern Pacific Railroad disputed that claim and filed a court case against him. The railroad won the court battle and then handed the land over to the federal government. The site was first officially established as "Lewis and Clark Cavern National Monument" on May 11, 1908,[5] but was not fully surveyed and declared until May 16, 1911, by President Taft as 160 acres (0.65 km2). The limestone cave is named after the explorers Meriwether Lewis and William Clark since the cavern overlooks over 50 miles (80 km) of the trail from the Lewis and Clark Expedition along the Jefferson River,[6] although Lewis and Clark never saw the cavern. Lewis and Clark did, however, pass through portions of the modern-day park. It is located approximately 45 miles (72 km) west of Bozeman, Montana, and 60 miles (97 km) northwest from the northwest corner of Yellowstone National Park. The caverns are also notable in that much of the work done to make the cave system accessible to tourists was performed by the New Deal-era Civilian Conservation Corps.[7]

It was disbanded as a national monument on August 24, 1937, because the National Park Service determined the caverns lacked the required national significance.[8] Ownership of the site was transferred to the state of Montana, and on April 22, 1938, Morrison Cave was declared Montana's first state park.[9][10] The site was formally dedicated in May 1941.[6][10] The park was listed on the National Register of Historic Places in 2018.[4]