Peter Moore, the former Liverpool chief executive, says the government’s handling of fans’ return to stadiums “poses an existential threat” to the English pyramid.
Clubs in the top six tiers of the English game must play behind-closed-doors until further notice.
In September, Prime Minister Boris Johnson announced that plans to allow fans to return to sport from 1 October would not go ahead.
It is now feared stadiums could remain closed for six months.
But while the government has said it will step in to help out the clubs in the three National League divisions, it is looking to the Premier League to provide the £250m it is estimated will be required to keep the 72 Football League clubs afloat.
On Friday, the Premier League announced games not selected for broadcast in October will be available to fans on a pay-per-view basis at a cost of £14.99 per game.
Speaking to BBC Sport, Moore – who left Liverpool in August after just over three years as chief executive – said the return of fans was paramount for the health of the game and predicted “carnage” if it does not happen.
“Everyone is struggling,” he said. “There is no doubt.
“I know the Department of Culture, Media and Sport (DCMS) is in a tough spot. But the government’s handling of the situation right now poses an existential threat to the football pyramid, particularly deep down in the pyramid where clubs have a different business model than the Premier League clubs who have the benefit of big media rights deals.”
Moore said he is worried about “the Scunthorpes, Grimsbys and Carlisles” of the football world.
“When I was a kid, I went everywhere with Wrexham in the old Third and Fourth Divisions,” he said. “I know what football means to communities. Particularly in the north, they are more than a sports enterprise. They are the heart and soul of that town or city.
“If we don’t get fans back into stadiums safely and securely soon, we are going to see carnage at the lower end of the football eco-system.”
Culture secretary Oliver Dowden has vowed to do everything he can to keep clubs afloat, while getting fans back into grounds soon and this week the Premier League, EFL and Football Association released a joint letter calling for supporters to be allowed back into stadiums.
Moore recently watched Bundesliga side RB Leipzig play in front of 8,500 fans at Red Bull Arena and says he can’t see why the same situation is proving impossible to implement in English football, particularly when some of the well known indoor venues in London, including the Royal Albert Hall, will be allowed audiences at events from December.
“There was a test event at Brighton in August, through which we learned so much and there was no evidence of a super-spreader,” he said. “Why do it if you are not going to act upon it?”
Moore also feels the government is missing a fundamental point in its demand for a lower-league bailout by Premier League clubs.
“It is not just the clubs, it is the hundreds of thousands of people who rely on clubs either for all their livelihood or to supplement it to get them by. Who is taking care of the people who no longer have the income they get from working as a steward?” he said.
“The Premier League will tell you it drives $3 or 4bn (£2.3-3.3bn) to the bottom line of the British economy. As someone who has lived abroad for 40 years, I know the Premier League does so much to enhance what people think for this country. The government has to recognise that.
“A plan needs to be built that brings people back to stadiums in a safe and secure manner because, whether it is mental health challenges or financial challenges, the collateral damage that is being done to the eco-system – and that is millions of people in this country – could be irreparable and long-term.”