Ayre, Liverpool's managing director, has argued the bigger clubs should get a greater share of the £1.4billion overseas TV cash - currently shared equally between all 20 clubs.
Manchester City, Manchester United, Arsenal and Chelsea are all understood to be against a change to the collective selling principle.
Manchester City chief communications officer Vicky Kloss said: "The subject has never been up for debate either inside the club or externally.
"We are well aware of the benefits of the collective selling of Premier League television rights."
United have always been a supporter of collective selling and chief executive David Gill told a Parliamentary committee earlier this year: "The collective selling of the television rights has clearly been a success and it has made things more competitive."
Whelan, meanwhile, has reacted with outrage.
He told Goal.com: "I have just read his [Ayre's] comments and I find them diabolical - I just can't believe what he has been saying.
"They are thinking 'how can we get more money?' You won't get more money by killing the heart and soul of the Premier League and killing the heart and soul of football in England.
"We invented the game and we have still got the finest league in the whole world and some of the finest supporters in the whole world and they want to rip the whole thing up."
Ayre pointed out that Barcelona and Real Madrid sell their own TV rights and earn considerably more, saying: "Is it right that the international rights are shared equally between all the clubs?
"At some point we feel there has to be some rebalance on that, because what we are actually doing is disadvantaging ourselves against other big European clubs."
Whelan added: "The worst thing for English football is for teams like Liverpool - the top four let's say - who want to get rid of virtually half the Premier League. We will finish up like the Spanish league with just two teams in it, no competition, no anything, no heart and soul in the league.
"What we have is the finest league in the whole world and what Liverpool are calling for would absolutely wreck it. The likes of Wigan, Bolton, Blackburn, Wolves, Sunderland and Newcastle couldn't compete."