The grant is believed to be £10m which will cover the lack of matchday revenue for the first three months of the 2020/2021 National League season, which finally got underway on Saturday.
The situation will then be reviewed and further financial assistance will depend on whether supporters have been allowed back into grounds.
How the money will be shared has not been announced yet but it is thought each club will receive a different amount after submitting paperwork detailing what their losses will be.
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The deal was announced on Friday, meaning the new National League season could start at the weekend – but Chesterfield’s match at Wealdstone was postponed due to a waterlogged pitch.
In a statement the National League said: “In recent weeks, the National League and the Football Association have been engaged with the government to address the revenue shortfall expected by member clubs caused by the pause to the safe return of spectators.
“The National League has now received confirmation of significant financial grant-aid support from the government to compensate clubs for essential revenue lost from fans not returning in October, and has communicated with its member clubs to provide reassurance ahead of the season start.”
The government paused plans to allow fans back into stadiums from October 1 due to the rising coronavirus infections across the country.
In other news, Chesterfield’s home games will be streamed online for £10 until supporters can return to the Technique Stadium.