The Old Course originally consisted of twenty- two holes, eleven out and eleven back. On completing a hole, the player teed up his ball within two club lengths of the previous hole, using a handful of sand scooped out from the hole to form a tee. In 1764, the Society of St Andrews Golfers, which later became the Royal and Ancient Golf Club, decided that some holes were too short and combined them. This reduced the course to eighteen holes and created what became the standard round of golf throughout the world.

The track through the whin bushes on which the Old Course evolved was so narrow that golfers played to the same holes going out and coming in. As the game became increasingly popular in the nineteenth century, golfers in different matches would find themselves playing to the same hole, but from opposite directions. To relieve the congestion, two holes were cut on each green, those for the first nine were equipped with a white flag and those for the second nine with a red flag.

When Old Tom Morris created a separate green for the first hole, it became possible to play the course in an anti-clockwise direction, rather than clockwise which had previously been the norm. For many years, the course was played clockwise an anti-clockwise on alternate weeks, but now the anti-clockwise, or right-hand circuit has become the accepted direction. Many of the course's 112 bunkers, however, are clearly designed to catch the wayward shots of golfers playing the course on the left-hand circuit.

The Open Championship was first played on the Old Course at St Andrews in 1873. With the 27th staging of the world's premier golf event taking place again on the Old Course in 2005, St Andrews has held the event more often than anywhere else. In modern times, the Dunhill Cup and the subsequent Dunhill Links Championship have been played at St Andrews since 1985, while the Walker Cup, the Amateur Championship and a host of other professional and amateur competitions for men and women have been held over the fabled links at the Home of Golf.