The Premier League said the golden handshake was proposed by its audit and remuneration committee and "supported and endorsed by the clubs". "It was vital that a comprehensive set of non-compete clauses were extended, to ensure the best possible protection for the future of the Premier League".
It was agreed that it is crucial for the League's ongoing success that Richard's unique knowledge and experience remain available in an advisory capacity.
And in a statement, umbrella group the FSF urged clubs not to contribute to a payment to Scudamore, who is leaving the Premier League after 19 years.
First mooted by Chelsea chairman Bruce Buck, a close ally of Scudamore's and the chairman of the audit and remuneration committee, the idea was labelled "hugely unpopular" by the Football Supporters' Federation.
"Premier League clubs have always told fan groups that budgets are planned in advance and there's not a surplus of cash lying around from their extremely lucrative TV deal".
"Now it appears clubs can stick their hands down the back of the sofa and find £250,000 at a moment's notice", it added.
That said, Scudamore has been paid considerably less than the bosses of the leading sports leagues in the United States and has turned down previous offers to earn more money elsewhere, most notably when he rejected the chance to run the global sports agency IMG a decade ago.
A statement on the club website reads: "The Premier League has today agreed the arrangements for Richard Scudamore stepping down from his role as Executive Chairman".
He has overseen a ginormous change in English football, which has seen the Premier League become the most watched league in the world.
The Premier League's British television rights were valued at £670 million when Scudamore took charge, but that figure has increased to £5.14 billion.