Fans of Kent-based , formerly Gravesend and Northfleet, paid £35 each to secure a £700,000 takeover of the club, which is sponsored by Eurostar, and plays in the same league as the likes of Exeter City, Rushden & Diamonds, and Torquay United.
The deal was masterminded by football fan forum , and means each fan who made a contribution to the acquisition will get a vote on player selections and transfers, and "all major decisions" affecting the club.
According to a BBC report, the acquisition of the 51% stake in the club will be completed in the next few weeks, while a further option to buy the club outright will be available to the team's backers.
It is understood to be the first time an English club has been bought in this way, and its announcement has already created opposing views within the football community.
Jason Botley, chairman of Ebbsfleet United, said the "extra finance and support will enable our club to progress", while it is expected that Liam Daish, manager, will stay on but in the new role of head coach.
However, David Sullivan, co-owner of Birmingham City FC, told the BBC: "I look forward to the experiment but I think it will be an utter disaster, although I could be very wrong.
Sullivan said fan involvement in team selection would cause trouble for the club's management: "If a player is in demand you need an instant decision, you can't go on the internet for six or 12 hours and let people vote.
"When you buy a player, you consider the transfer fee, the agent's fee, and their wages. But those details are confidential and unless fans have that information you can't make a rational decision."
Daish, who is a former international for the Republic of Ireland, said: "As a football fan I think the idea is fantastic. I look forward to the challenge of working with thousands of members to produce a winning team."