Rybolovlev, aged 47, has to give Elena Rybolovleva, who was with him for 24 years, exactly 4,020,555,987 Swiss francs and 20 centimes (€3,289,249,531.62).
After a six-year divorce battle, Ms Rybolovleva has won what is thought to be the world’s biggest settlement.
The proceedings came about when she stunned her husband by filing a divorce petition on New Year’s Eve 2008 and had his accounts frozen.
She claimed his infidelities had ended their relationship and gave written testimony of parties on yachts where, she said, he shared some “young conquests with his friends, and other oligarchs”.
Elena Rybolovleva, who met her husband more than 30 years ago, when they were students in the Ural mountains, won custody of the couple’s 13-year-old daughter, although her estranged husband can still appeal the ruling.
She began divorce proceedings by winning a freeze on some of her husband’s assets including his majority ownership in French soccer club AS Monaco, a $295m stake in Bank of Cyprus, and a $95m Palm Beach home bought from Donald Trump.
She later sued him in the United States, accusing him of trying to shield the Florida property from the divorce proceedings, along with an $88m Manhattan penthouse.
She also said her husband had used marital property to buy a multitude of other assets through a variety of trusts and limited liability companies, hoping to put those assets beyond her reach.
Last year their elder daughter Ekaterina bought the Greek resort island of Skorpios, where shipping tycoon Aristotle Onassis married Jacqueline Kennedy in the 1960s.
She bought the island from Onassis’ granddaughter Athina Onassis Roussel.
Mr Rybolovlev, who is resident in Monaco, made much of his fortune from the 2010 sale of his stake in fertiliser company Uralkali for $6.5bn.
In a statement her lawyer Marc Bonnant called it “the most expensive divorce in history” — an unheard-of amount for Switzerland and for Russian oligarchs — but noted the judgement could be appealed.
Mr Rybolovlev’s wife had demanded $6bn from the man known as the “fertiliser king”, whose fortune from potash mining made him the world’s 79th richest person. Forbes estimates his worth at $8.8bn.
His Geneva lawyer did not comment.
Other properties Mr Rybolovlev owns include a $21m Hawaii mansion he bought from the Hollywood star Will Smith, and the La Belle Epoque penthouse in Monaco, where he lives, for which he reportedly paid $320m.
Mr Rybolovlev’s art collection includes Picassos, Van Goghs, Gauguins and Monets.
It is the latest chapter in the bizarre lives of the ex-couple. In February Elena was quizzed by Cyprus on suspicion of stealing a diamond ring worth $27m, borrowed from her daughter but not returned, and which belonged to a trust. She was later released without charge.
Mr Rybolovlev, once spent 11 months in jail — accused of murdering a competitor — before the charges were dropped.
The settlement dwarves the €1.84bn paid by art heir Alec Wildenstein to ex-wife Jocelyne.
Media mogul Rupert Murdoch was ordered to pay his former wife Anna €1.23bn in 1999.
He went on to marry his third wife Wendi Deng, from whom he is now divorced.