The 60-year-old golfing legend won two of his three Open titles at the east-coast links, adding to the title he claimed at Muirfield in 1966.
His double leaves him standing proud alongside Sam Snead, Peter Thomson, Seve Ballesteros and Nick Faldo in the St Andrews Open winners' enclosure.
He is also one of only four players to have claimed the modern Grand Slam, joining Ben Hogan, Gene Sarazen and Gary Player, though Tiger Woods could join that exclusive club with a win at St Andrews.
Just like his emotional farewell to the US Open last month, Nicklaus is likely to treasure every walk down every fairway at St Andrews as he recalls his two glorious triumphs.
In 1970, though, victory had not looked on the cards as Doug Sanders kept his nose in front on the final day.
Sanders needed only a four at the last to become the first pre-qualifier to win the tournament.
With Old Tom's 18th regarded as the easiest par four on the course, the trophy was well within Sanders' reach, but he missed a four-foot putt to secure the title and was left to face a play-off.
The 18-hole play-off took the championship into a Sunday for the first time and Nicklaus dominated as Sanders' near miss haunted him 24 hours on - as it would do for a lifetime afterwards.
Nicklaus was four up after 13 holes and, although his rival fought back, a monster drive in excess of 350 yards at the last ensured Nicklaus was not going to make the same mistake Sanders had made.
He duly made his par to secure his second Open crown and his first on The Old Course.
Nicklaus returned triumphant to St Andrews in 1978, coming from two shots behind third-round leader Peter Oosterhuis to claim his third Open title.
But again The Golden Bear had to produce a golden finish as playing partner Simon Owen chipped in at the 15th to edge ahead by one shot with three holes to play.
He pulled a further shot clear at 17 and closed out in his now traditional manner at 18 to add to his mounting collection of Majors.
Nicklaus now boasts a record 18 Majors, but the fact you need to go back 14 years for his last underlines part of the reason that this season is becoming something of a farewell tour.
Nicklaus has come under fire for being handed too many tournament exemptions, not least from US Golf Association executive director Frank Hannigan, who recently accused the US Open of "nostalgia, weepy sentimentality and cheap popularity over fairness".
Whatever the reason, the exemptions are beginning to dry up and Nicklaus's chances of qualifying in his own right are growing slimmer each year, so who can blame him for savouring the moment?