Prestwick Golf Club was founded in 1851 by a group of 57 members who met at the Red Lion Inn, Prestwick. The Earl of Eglinton was the first Captain of the club, and presented a gold medal for annual competition, the Eglinton gold medal is still played for to this day. Colonel Fairlie of Coodham brought Tom Morris with his wife Agnes and son young Tommy to Prestwick from St. Andrews, to be the Keeper of the Green, Ball and Club Maker. The members purchased two cottages opposite the Red Lion Inn- One for Tom, and the other as a clubhouse- both buildings are still standing today albeit visibly reconstructed. Tom returned to St.Andrews in 1864 and his house was auctioned in 1866 for £170. This allowed the club to build a new Clubhouse on the present site for a cost of £758 in 1868. In 1877, extensions cost £700 and in 1882, 90 lockers, which are still in use, were installed at a cost of £350. A major re-development was completed in 1999.

The first Open Championship was held at Prestwick in 1860, which was organised by the members who subscribed £25 to purchase a red morocco belt with silver clasps. It was won by Willie Park of Musselburgh with a score of 174 over 36 holes and there was no prize money. The Belt was won in three successive years by Young Tom Morris from 1868 to 1870 and thus became his property. When Morris won for the third time, in 1870, he had a first round score of 47 over 12 holes, a score that has never been equalled or bettered. He started with a three at the 578 yard first hole- in those days a par 6. His Belt is now in the keeping of the Royal and Ancient Golf Club of St.Andrews. A replica Belt was presented to Sandy Lyle, the winner of the 125th Anniversary Open Championship at Royal St.Georges Golf Club. Another Belt is on display in the Cardinal room in the Prestwick clubhouse. There was no Championship in 1871 and, and thereafter, Prestwick, the Royal and Ancient Golf Club of St.Andrews, and the Honourable Company of Edinburgh Golfers joined forces to purchase a current Claret Jug for £30, played for in the Open Championship. When the Championship was revived in 1872 Young Tom won again, thus winning the Open four times in a row- a feat no other golfer has ever matched, or likely will. His prize money was £8.

Prestwick hosted the Open twelve more times after 1872, from 1875 intermittently until 1925. It was in 1182 that the eighteen hole course was born. Notable winners during this period included John Ball Jr., the first amateur to win the Open – the last amateur to win being the legendary Bobby Jones, in 1930 at Hoylake. Harry Vardon, who won the Open a record six times, won at Prestwick on three of those occasions; in 1898, 1903, and 1914. In 1908, James Braid, a member of the great golfing triumvirate, won at Prestwick, and he was also involved in the redesign of parts of the course, a role he was to fulfil for many other courses thereafter.

Prestwick’s final Open was in 1925, when the crowds became so great that players were insufficiently protected, and MacDonald Smith in particular, was put off his game, allowing Jim Barnes USA to steal the title.

The Amateur Championship has been held at Prestwick on eleven occasions from 1888 to 2001, in which year Michael Hoey was the Champion. The most remarkable final was between W. Lawson Little Junior of Presidio, USA and J. Wallace of Troon Portland in 1934. Little went round in 66 in the morning and started in the afternoon 3 3 4 3 3, to win at the 5th hole by 14 and 13. In 1952 the final of the Amateur Championship was between two Americans - Frank Stranahan and winner Harvie Ward. The last Amateur held at Prestwick was 2001 as part of the Celebrations for the Club's 150th Anniversary. It was won by Michael Hoey from Shandon Park, Northern Ireland, who defeated Ian Campbell from Marlborough Golf Club in Wiltshire, by one hole in a closely contested final. A new amateur course record of 66 was set by Nick Dougherty of Shawhill.

A stone cairn to the west of the Clubhouse, marks the first tee of the original 12 hole course, from which the first Open was played. The 1st hole measured 578 yards to what is now the 16th green, where in 1870 Tom Morris Jr holed out in three strokes using hickory shafts and a gutty golf ball. Seven of the original greens are still played on today. The Cardinal Bunker is named after "The Cardinal's Nob (or nose)', a monk of Crossraguel Abbey (now a ruin -near Turnberry) played a match to settle a deadly feud against a Lord of Culzean -the wager, his nose. Willie Campbell's grave is a bunker on the current 16th hole where Willie, leading in the Open of 1887, took four shots to escape, and in doing so, lost the Championship to Willie Park Jr. The Elysian Fields comprise the fairways to the east of the Pow burn and to the north of the Dow burn. The Zareba is the hollow near the Cardinal under the shoulder of the 16th green. The Hartz Mountains constitute the rolling 13th fairway, named after Harry Hart the Secretary (left), who was so short he would periodically appear 'invisible' on the 13th.

When Tom Morris Snr left the Club for St. Andrews in 1864, Charlie Hunter then took his place, but left soon after for Blackheath in 1865. On his departure, Andrew Strath of St. Andrews, then took the post of Keeper of the Links in 1865, the same year he won the Challenge Belt. Strath died tragically in 1868 of tuberculosis at the age of 32. Charlie Hunter then returned from Blackheath to become Custodian of the Links. Hunter, competed in, or was the official starter at every Open Championship at Prestwick until his death in 1921 with 53 years service to the Club. A portrait of Hunter hangs in the Dining room (right). James McDowall then became the club professional for a term of 6 years resigning in 1927 when Robert McInnes was appointed. McInnes became an Honorary Member in 1957 and died in 1962. Frank Rennie (left) was appointed in 1962 and remained in post for 42 years until he retired in 2004. Frank was made an Honorary Life Member in 1988.

David Fleming succeeded Frank and was appointed Professional in October 2004. David trained at Turnberry and became Head Professional. He then became Director of Golf at Carton House, Dublin prior to his appointment at Prestwick.