She said this evening she had "great sadness" at having to resign from her job because of "registered interests" delaying the policy to cut the max bet from £100 to £2.
The MP for Chatham and Aylesbury said on Twitter: "Politicians come and go but principles stay with us forever."
In her resignation letter she lashed out at the delays to the new policy, saying two people die every day due to addictive gambling and she simply couldn't support any further delays.
Ms Crouch said to the PM: "This delay is unjustifiable… there is no reason why implementation cannot come in sooner than October".
She went on: "It is a fact of Government that ministers cannot disagree with policy, let alone when it is policy made against your wishes relating to your own portfolio…
"I hope you understand my position and accept my resignation with the sadness it is tendered."
MPs from across the political spectrum spoke out to pay tribute to her work in Government.
Labour's Tom Watson said she had taken a "courageous and principles decision" and had "poured her heart and soul into a significant review of these destructive machines".
Tory MP Iain Duncan Smith said he was "desperately sorry" she'd left the Government.
He told Sky News: "There is support from all sides of the House on this… They want it to happen and at the earliest opportunity. We need to place humans above money."
And David Lammy added: "You can hold your head high. Well done for putting principle ahead of ambition."
Just hours before she quit Culture Secretary Jeremy Wright had said she was "doing an outstanding job as minister for sports and civil society".
He said today that there was "no delay" to the plans to slash the max spin down, but they won't come into effect until October.
But critics said Mrs May was guilty of helping to perpetuate the burning injustices she said she was determined to tackle in office.
Chief Secretary to the Treasury Liz Truss tried to reassure her by saying ministers had "brought the date forward for the FOBT by six months" already to October 2019 and was happy to meet to discuss it – but MPs weren't happy with that.
The delay protects jobs and government revenue they get from taxing the bets. And the extra time will hand bookies an extra £900million.
But MPs slammed the decision, calling the fixed odds betting machines a "scourge" on society.
The machines, known as FOBTs, are a huge source of revenue for high-street bookies – but campaigners say they target gambling addicts.
Shop closures are expected after the change comes into play – and shares dropped 10 per cent in Ladbrokes on the news when it was announced earlier this year.
Today Iain Duncan Smith demanded ministers bring forward the change earlier than planned. He stormed: "It's not too late. For the sake of those people whose families and lives have been destroyed – and there may yet be more of them – I urge my honourable friend to think again and bring forward the date so we can end this scourge".
Today the culture minister had crunch meetings with the chief whip over the issue.
She was rumoured to be on the verge of resigning over it for days.
But No 10 had no knowledge this lunchtime that she'd quit.
Downing Street said the October deadline was "a balance between making sure we protect those who work in the industry and making sure that we bring in this really important change".
Earlier this week online gamblers were hit when the Chancellor pushed up remote gaming duty by 6 per cent – that'll come into place in October next year.
The extra revenue will likely help pay for the FOBT crackdown.
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