A wholesale review of the way English football is run will consider creating a new regulator, changing the "fit and proper person test" for owners and examine how to give fans a greater say in how their clubs are run.
The review, ordered in the wake of the European Super League debacle, will also consider interventions to protect clubs' identities – including their location and team badges.
Ministers hope the doomed breakaway bid by the so-called 'big six' teams will prove to be a "watershed moment" for the national game, creating a new environment where fans have a greater say.
Former sports minister Tracey Crouch will lead the work, which could result in new laws being passed to improve the governance of the sport.
The widely condemned European Super League proposals involving Arsenal, Chelsea, Liverpool, Manchester City, Manchester United and Tottenham were the catalyst for the launch of the review.
But it will examine wider questions about the way the sport is run, looking at examples such as the collapse of Bury Football Club, which went into administration last year having been expelled from the English Football League in 2019 due to financial problems.
Sports minister Nigel Huddleston said: "Football begins and ends with fans and we have seen that passionately displayed this week. It must be a watershed moment in our national game.
"We must capitalise on this momentum. Clubs are the beating heart of their local communities and this important review will help put football on a surer footing for the future where supporters' voices are heard."
The review will examine the way the game is run overseas, such as Germany's Bundesliga where teams are only allowed to take part if commercial investors hold no more than a 49 per cent stake in their ownership, giving fans a major say in the running of their clubs.
It will examine whether the existing owners' and directors' tests are fit for purpose and consider whether additional criteria should be added.
The review will also look at whether oversight of foreign ownership of clubs is sufficient to protect the interests of the game.
Ms Crouch said: "Football means so much to so many people in this country and my review will be firmly focused on the fans.
"It will look closely at the issues of governance, ownership and finance and take the necessary steps to retain the game's integrity, competitiveness and, most importantly, the bond that clubs have with its supporters and the local community."
The review will investigate whether administrators could better scrutinise clubs' finances on a regular basis and examine how money flows through the football pyramid, including solidarity and parachute payments and broadcasting revenue.
Ministers will work with Ms Crouch to set out the next steps in the review in the coming days.
Ms Crouch's review will be presented to Mr Huddleston and Culture Secretary Oliver Dowden, along with the Football Association, before being laid in Parliament.
Malcolm Clarke, chair of the Football Supporters' Association, described the actions of the 'big six' as "the best own goal we've ever seen" and welcomed the review.
"The owners of the big six have shown how powerful they are – their plans were so awful that within 24 hours a fan-led review that will look at the very power structures of football was announced," he said. "It's the best own goal we've ever seen.
"We welcome the release of the Terms of Reference and look forward to supporters being at the absolute heart of this review. The status quo cannot continue and we will demand change."