The decision is a defeat for the 85-year-old, who bought the club in 1988 but has been embroiled in a bitter dispute with former business partner and club president Valeri Belokon for several years, and it will be celebrated by Blackpool fans.
But it comes with the risk of the English Football League's 12-point penalty for clubs that experience an "insolvency event" - a measure designed to prevent clubs from gaining an unfair advantage by living beyond their means.
Blackpool's case, however, is different to most of football's other recent financial crises as the club is not insolvent and is now in the hands of receivers, not administrators.
A receiver is appointed on behalf of a particular creditor, while administrators are appointed by the court to stop any further losses or wind up the business.
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A 12-point deduction, if it was applied, would see Blackpool fall from eighth place to 17th, just two points above the relegation zone.
In a statement, EFL chief executive Shaun Harvey said: "The EFL notes today's developments in regard to Blackpool Football Club following the hearing in the High Court.
"The matter will now be considered by the EFL Board at the earliest opportunity (March 6) and we will be seeking an early meeting with the receiver, so as to ensure that the best interests of the club can be jointly considered, against the context of our regulatory framework."
Many Blackpool fans will consider a 12-point penalty as a small price to pay for lifting the cloud over Bloomfield Road.
Belokon successfully sued Oyston and his son Karl, the club's ex-chief executive, in 2017 after discovering that they had "asset-stripped" Blackpool by paying themselves huge bonuses and salaries following the club's season in the Premier League in 2010/11.
The Latvian banker was awarded £35million but - 15 months and several missed deadlines later - he has received only £10million of that sum, while Oyston refused to sell the club.
That decision is now out of his hands, though, as Justice Marcus Smith agreed with Belokon's lawyers that the club should be handed over to Paul Cooper and David Rubin from the insolvency firm David Rubin and Partners to force through a sale.
In a statement released to Press Association Sport, Cooper said: "We are only too aware of the history of Blackpool Football Club, the central part the club plays in the community and the emotions involved for those supporters dedicated to securing its future.
"This has obviously been an unsettling period in the club's history. But, in this time of uncertainty, the joint receivers will be doing everything in their power to keep the fans informed of relevant developments."
The Tangerines have officially been on the market for more than a year and are currently losing about £2million a season, mainly because a large section of supporters have been boycotting the club.
PA Sport understands there are at least two groups interested in buying the club, which is estimated to be worth between £10-12million. One of those groups is fronted by former Blackpool and England player Paul Stewart.
These interested parties, and others before them, have all been frustrated by a combination of Oyston's reluctance to sell, his unreasonable valuation of the club and Belokon's own status as a potential minority shareholder.
He would not currently pass the EFL's Owners' and Directors' Test, owing to a money-laundering and tax evasion conviction he received in Kyrgyzstan in 2017.
Belokon has always denied those charges, saying the prosecution was politically motivated. It is understood that he has made submissions to the EFL and they are being reviewed.