The racetrack, leased from the Council by the committee of the Western Meeting, was on an area of common land near Belleisle estate, and for some years, local people had played golf there on an unauthorised course they had created. The Council decided to lay out a proper course, and Charles Hunter of Prestwick Golf Club was brought in to do this. The opening ceremony was performed by the daughter of Provost William Allan, and an exhibition game was then played between John Hunter of Prestwick and David Kinnell, golf club maker and professional at Prestwick St Nicholas, with Kinnell winning. In 1907 horse racing was transferred to the present racecourse. The Council then acquired the grandstand of the old racecourse for conversion to a clubhouse, dismantled the racetrack railings, and rearranged the golf course, extending it to eighteen holes.

The course was of no particular distinction, and space was restricted, but golf was so popular with locals and visitors that it was frequently overcrowded. Various schemes for a new golf course were considered, but no suitable land could be found until Belleisle estate came on the market in 1926. The Council purchased the estate, and James Braid, five-time Open Championship winner and celebrated golf course architect, was invited to design the courses. Two courses were planned, No. 1 which became known as Belleisle, and No. 2, incorporating part of the old course, which became known as Seafield. The Council approved Braid’s plan, and the construction contract was awarded to the firm of John R. Stutt of Paisley. (Braid and Stutt often worked closely together in golf course construction.) Clubhouse facilities were installed in part of the basement floor of Belleisle mansion house, and the remaining grounds of the estate were laid out as a public park. The cost of the golf courses was around £5,000.

Both courses were officially opened on Saturday 10 September, 1927, Provost James Gould driving the first ball from the first tee on each course in front of a large crowd. Exhibition matches were played between James Braid and Alexander ‘Sandy’ Herd – another veteran Scottish professional and Open Championship winner (1902) – on one side and two local amateurs, the Reverend David Rutherford, minister of Ochiltree, and Allan Raeside, of Ayr Municipal Golf Club, on the other side. The amateurs won the morning match on the Seafield course, and the professionals won the afternoon match on the Belleisle course. During the interval, Provost Gould presided over a luncheon for a large number of guests including local dignitaries and representatives of Ayrshire golf clubs. Two silver trophies were exhibited, one presented by Sir Archibald Walker of Newark Castle and the other by the contractor, John R. Stutt. These were to be competed for annually.

The 1936 Penfold Golf Tournament was played at Belleisle on 15, 16 and 17 June. It was won by Troon-born James ‘Jimmy’ Adams, who shortly afterwards came second in the Open Championship at Hoylake. Tom Collinge came second. Percy Alliss, who came third, set a new course record of 69.

During the Second World War, when Germany’s U-Boat campaign threatened Britain with starvation, the Belleisle course was ploughed up and used to grow food. It was reinstated after the war by the original contractors, Messers Stutt & Co. of Paisley at a cost of £2,000. It was re-opened on 4 June 1949 when an exhibition match was played between the pairing of John Panton, Scottish Professional Champion and Hamilton McInally, three times Scottish Amateur Champion, against Jimmy Adams the 1936 Penfold winner and Victor Finlayson, the Belleisle Club Champion. (Panton and McInally won.)

The 1963 Swallow-Penfold Golf Tournament was played at Belleisle. It was won by Bernard Hunt.

In 1978, when the Open Championship was played at Turnberry, Belleisle hosted the qualifying rounds.