The Old Course at St Andrews is considered by many to be the "home of golf" because the sport was first played on the Links at St Andrews in the early 15th century. Golf was becoming increasingly popular in Scotland until James II of Scotland banned the game in 1457 because he felt that young men were playing too much golf instead of practising their archery. The ban was upheld by James III, and remained in force until 1502, when James IV became a golfer himself and removed the ban.

In 1552, Archbishop John Hamilton gave the townspeople of St. Andrews the right to play on the links. In 1754, 22 noblemen, professors, and landowners founded the Society of St Andrews Golfers. This society would eventually become the precursor to the Royal and Ancient which is the governing body for golf everywhere outside of the United States and Mexico. St Andrews Links had a scare when they went bankrupt in 1797. The Town Council of St. Andrews decided to allow rabbit farming on the golf course to challenge golf for popularity. Twenty years of legal battling between the golfers and rabbit farmers ended in 1821 when a local landowner and golfer named James Cheape of Strathtyrum bought the land and is credited with saving the links for golf.

The course evolved without the help of any one architect for many years, though notable contributions to its design were made by Daw Anderson in the 1850s and Old Tom Morris (1865–1908), who designed the 1st and 18th holes. Originally, it was played over the same set of fairways out and back to the same holes. As interest in the game increased, groups of golfers would often be playing the same hole, but going in different directions.