So, what the Premier League chief executive, Richard Scudamore, must have thought would never happen, to a gilded club reaping the riches he delivers for them, has finally befallen Portsmouth. Since the Premier League was formed in 1992, as a breakaway by the then First Division clubs so they would not have to share their forthcoming satellite TV bonanza with the other three divisions, Football League clubs have collapsed insolvent, usually into administration, 53 times.

It has become a grim part of the job at Football League headquarters to talk to administrators, deal with millions of pounds unpaid to people who dealt in good faith with the historic names of English football, and worry whether clubs' carcasses will be bought up and some financial life breathed into them. Now Scudamore, between negotiating another bumper round of new international TV deals for 2010-13, will have to spend time himself contemplating a furious HM Revenue & Customs with unpaid Pompey tax bills, fret over whether the club will be bought at a knockdown price and survive, and approve football's dire system of insisting millionaire players are paid in full while ordinary businesses, public bodies and the tax man are left high and dry.

Around the world, even as crowds still thrill over the action served up by the world's richest league and broadcasters prepare to pay a total understood to be around £1.1bn for the TV rights, this season's Premier League table will forever show an asterisk next to one of the 20 clubs, with nine points deducted, for falling into financial ruin.

The Premier League rejects the idea that this is a major embarrassment that should prompt a bout of soul-searching. Portsmouth's collapse is due to rank bad management and overspending, they say. That is true, and it is the administrator's job to decide whether the problem results from even worse practices than that. But as far as we know, Portsmouth did nothing against any rules; they followed the accepted Premier League model for a club – overspending, beyond the club's true means, financed by loans from an owner and banks.

Portsmouth's core problem at the end of Sacha Gaydamak's ownership last summer was that he, who had passed the fit and proper person test and satisfied the league he owned the club rather than his father, the now convicted gun-runner Arkadi Gaydamak, had become simply not rich enough. Then the overspending became unsupportable and Pompey, three owners later, have collapsed.

The latest, Balram Chainrai, loaned money, apparently £17m, into the club in return for mortgages on Fratton Park and the club itself, and it should be noted that this gives him priority to be repaid first and, most likely, emerge again as Portsmouth's owner. The players have to be paid in full for the club to be allowed to continue, and the "ordinary" creditors, again, will be paid a fraction of what they are owed. That is what infuriates HMRC about football clubs, and the tax authorities are certain to be left short again.

This vulnerability in the game's makeup, the reliance on owners, was precisely identified by the FA chairman, Lord Triesman, in his famous speech at the Leaders in Football conference of October 2008, in his early days, when he believed his job was to help pull the game into some agreed order. "Debt is at high risk levels," he said. "The clubs are owned by either financial institutions, some of which are in terrible health, or very rich owners who are not bound to stay, or not very rich owners who are also not bound to stay."

For speaking that truth in public he was vilified, and even as Portsmouth, among others, have proved his warning right, Triesman has not felt able to speak out again or gather support for solid action.

The Premier League points to new rules it introduced last summer, including a "going concern" test by which accountants will examine future financial projections for a club. It is not clear these go far enough, because while Gaydamak was putting the money in and banks were lending, Pompey, coming back with the FA Cup on an open-top bus, presumably looked healthy enough into a foreseeable future.

Uefa have moved, introducing their "financial fair play" initiative, which will require clubs to be breaking even from 2012-13, an act of almost heartbreakingly simple leadership. The Premier League does agree but argues that owners should still be allowed to take over clubs and put money in to fund overspending. That, though, is the inflationary lottery Uefa is seeking to solve.

At Manchester United and Liverpool, the takeovers have loaded the great clubs up with debts. At the clubs with owners putting money in, some are rich enough to sustain it, and do it relatively responsibly. It does, though, inflate players' wages at all clubs, fuelling overspending. At some, Pompey now proving the point, the commitment will become too great once rich men pull out.

In the Football League, many of the insolvencies have been caused partly by the huge financial gap with the breakaway Premier League. Now, the freewheeling way the great game is organised has finally claimed a victim in that golden circle, with Portsmouth, established in 1898, becoming, in 2010, the first club in the multibillion-pound Premier League to file for insolvency.