The Hamilton Grand development has become so sought after that it has set a new top price of Â£2,490 per square foot.
The news comes a year after the high prices paid for flats in the former hotel led to the street being named as the most expensive in Scotland.
The 122-year-old building, which opened as the Grand Hotel, has been converted into 26 luxury flats by estates firm Kohler & Co over the last seven years.
They have been put up for sale at asking prices starting at Â£1.05m for a two-bedroom apartment and from Â£4.1m for a four bedroom one.
The Bank of Scotland said the average property sale price in The Scores, where the complex is situated at its corner with Golf Place, was Â£2,179,000 last year.
Estate agents Savills said new figures were due out soon.
Spokesman Jamie Macnab said: "Golfers from all over the world want to play the Old Course, and many fall in love with the historic coastal university town and dream of buying a home here.
"Hamilton Grand has attracted buyers from all over the world, including America, Scandinavia and Hong Kong.
"To date, all the buyers have been from abroad, including ex-pat Scots.
"We now look forward to finding buyers for the premier, four-bedroom apartments on the top floors of the building, where views over the Royal and Ancient Golf Club and the Old Course, as well as over the West Sands and out to sea, are beyond comparison."
The hotel operated as a St Andrews University halls of residence for 56 years until 2004.
Kohler & Co, which owns The Old Course Hotel, Golf Resort and Spa, bought the disused building in 2010, adding an extra floor.
Bank of Scotland mortgage director Graham Blair said: "Living on the coast offers many attractions, including a typically high quality of life and attractive surroundings.
"As a result, property in seaside towns is often very popular with homebuyers.
“Over the past ten years, the strongest performing seaside towns have been on the Aberdeenshire coastline, as the oil industry was experiencing its boom period.
"However, more recently, house price growth has slowed down in many coastal towns, meaning good value for money can be found for those searching to realise their dream of living near the sea."