Royal Troon began in 1878 with five holes scratched out of the dunes south of the town. By 1884 the original course had grown to eighteen, designed by the club's first professional George Strath in partnership with Willie Fernie, who had won the 1883 Open Championship. Charlie Hunter, the greenkeeper at the neighbouring Prestwick Golf Club, helped them lay it out. When Strath left in 1887, Fernie took over as head professional and held the post until his death in 1924 - thirty-seven years of shaping a course he had helped to design. He laid out what would become Troon's New Course; Alister MacKenzie redesigned it in 1921, and it was renamed shortly after in honour of the 6th Duke of Portland, one of the region's largest landowners and an early patron. Today the club has forty-five holes across three layouts - Old, Portland, and the nine-hole par-3 Craigend - on a links that runs along the Firth of Clyde.

The Open Championship arrived at Troon in 1923 and has returned ten times. The course was granted its Royal designation in 1978, the year of its centenary. The clubhouse, built in 1886 to a design by Henry Edward Clifford, holds an astonishing collection of historical golf artifacts - silver-headed clubs, championship belts, photographs of players in tweed plus-fours from a vanished century. James Montgomerie, father of the modern champion Colin Montgomerie, served as Secretary in the 1980s. The course has lengthened over the decades to keep pace with the modern game. The 1950 Open played at 6,583 yards. The 2024 Open played at 7,385 yards, a difference of more than eight hundred yards in the same routing. Players go further now; the wind off the Firth still does not care.

On 1 July 2016, a few weeks before the Open Championship returned to Troon, the club's members voted overwhelmingly to admit women as members for the first time in its history. The R&A had already made clear that clubs which excluded women would lose their place on the Open rota. Royal Troon's vote ended the controversy before the championship arrived, but it also closed a long chapter. In 2020 the club hosted the Women's British Open - the only major it has held in a year without a men's equivalent, and the eleventh Open Championship of any kind to be contested on its fairways. The same dunes, the same gorse, the same Postage Stamp. Different competitors, finally.

The par-5 sixth, called Turnberry, runs six hundred and one yards along the railway line - until 2023 it was the longest hole in Open Championship history, eventually surpassed by the par-5 fifteenth at Royal Liverpool. Two holes later comes the Postage Stamp eighth, where a slightly mishit ball funnels into the Coffin bunker and disappears. Then the eleventh, the Railway, which the statisticians sometimes claim is the hardest hole in major championship golf - a blind drive over gorse to a fairway that tightens as it goes, an approach to a green that runs away, out-of-bounds an inch from your left shoulder. Players who emerge with par on the Railway look back at it the way climbers look back at summits. The 1962 through 1989 Opens played it as a par-5, which softened the brutality. Now it is a long par-4. The course architects took the kindness away.