Lawyers say the low-cost carrier could be liable for payouts of around £610m (€847.02m) after the firm lost a test case at Manchester County Court.
Ryanair, however, disputes this figure and claims that its liability, should it lose its appeal, is likely to be less than €5m.
The airline had argued claims for delays could be limited to two years under a clause in their terms and conditions small print, not six years, as is the rule under European Union law.
The case was brought by lawyers for six delayed passengers who tried to claim compensation for delayed flights after five years and eight months, which Ryanair contested.
After a long-running legal battle, Judge Platts ruled Ryanair’s rules fall foul of European Flight Delay law.
Ryanair said it will appeal the decision.
Lawyers say the ruling in the case, Goel & Trivedi v Ryanair, stands to affect millions of air passengers.
They say if Ryanair had won, all airlines might have been able to put a two-year time bar on all existing and future flight delay claims.
Kevin Clarke, lawyer for Manchester law firm Bott & Co, who fought the case for the passengers, said: “We’re delighted that the court has dismissed yet another argument put forward by the airlines to restrict passenger rights.
“The Supreme Court decision last year said passengers have six years to bring a claim. That is a definitive, binding, clear judgment from the highest court in England and Wales.
“This should have concluded matters but unfortunately Ryanair have been able to tweak the argument; we found ourselves running a complicated court case arguing the fine points of contract law."
In a statement, Ryanair said: “We note this ruling which reverses Lower Court orders that a two-year time limit for claims is reasonable.
“Since we believe a six-year time limit for submitting such claims is both unnecessary and unreasonable, we have instructed our lawyers to immediately appeal this ruling.
“Ryanair today rubbished the absurd claims about its potential liability under the Manchester Court judgement.
"Firstly, since less than 1% of Ryanair flights are delayed over three hours and since more than 90% of passengers make a valid claim within Ryanair’s contractual two-year period, there is a tiny potential group of passengers who may wish to submit a claim between two and six years after the date of their flight delay.
“Accordingly, Ryanair estimates that even if its appeal in this matter is ultimately unsuccessful, its potential liability will not be material and is likely to be less than €5m.”
However, the lawyers insisted their estimates are accurate.
Mr Clarke said the figures were based on the possibility that everybody who could claim would do so.
“The figure we have provided is accurate,” he said.
“Ryanair say that more than 90% of people who make valid claims with them do so within two years. However, only a fraction of people who can claim do claim and as such this point is ultimately specious.
"This is the only accurate, unbiased statistic which matters. It is their total liability.”
Ryanair’s share price fell 3.65% to €12.05 yesterday.