Premier League clubs could afford to make cuts of up to £32 to the current ticket prices set, according to the Football Supporters' Federation.
Manchester City have sent back 900 tickets to Arsenal as some supporters boycott their match on Sunday in protest at the £62 cost of a brief.
Chelsea, Liverpool, Manchester United and Tottenham Hotspur fans are also charged the same amount because they fall under Arsenal's Category A list.
City's success in the last two years, in which they ended 35 years without a major trophy, usurped Arsenal in the Premier League and then became champions for the first time in 44 years, has elevated them into the A group.
Stoke City fans will pay £35.50 when their side travel to Arsenal next month and the Football Supporters' Federation chairman Malcolm Clarke believes there is no justification for such pricing structures.
"We have not done the final calculations but we estimate clubs could cut £32 off the cost of every single ticket purely from the increase in the TV pot this time around," he said.
"I know the clubs make the argument of needing the money to attract the biggest stars but I think I know what even Manchester City fans - with their large and enthusiastic following - would go for if they were given the choice of lower ticket prices or slightly worse players than they have now."
Clubs are now set to benefit from the Premier League's lucrative TV deals, including overseas rights, which has crashed through the £4billion barrier.
Often described as "the best league in the world", the Premier League has however alienated a core set of supporters across the country united in their disgust at English football's commercialisation and the catering for bandwagon-jumpers ahead of sussed supporters.
"There are many ways of measuring what is the best league," Clarke explained. "But if you look at the Bundesliga, where fans can attend matches for €15, stand up, have a pint if they wish, and even get a ticket for the metrolink, it seems the Premier League is short changing its own supporters.
"This business of categorising matches is blatantly unfair. Just because Manchester City have a lot of money doesn't mean their supporters have, and the same is true of the other teams who get charged the highest prices every time they play.
"And if they are starting to say enough is enough, and that in turn affects the atmosphere within the stadiums, will it retain its worldwide popularity? I am not so sure it will.
"This is a real test for the Premier League.
"They seem to think football is immune from the economic situation elsewhere. But it isn't. And how it responds - especially next year - will shape the game for years to come."
The half-and-half scarf culture which has infested English football is symptomatic of the plight of atmospheres and clubs' support, and Clarke believes there is a risk of an entire generation being lost to the game.
"According to the Premier League's own figures, the average age of fans is going up all the time," said Clarke.
"If it is far cheaper to spend the afternoon in the pub, where is the incentive to attend matches? And once people get out of the habit of going to games, it is not easy to get it back." end