The departures of Maria Caulfield and Ben Bradley heaped more pressure on the Prime Minister a day after she managed to survive the resignations of foreign secretary Boris Johnson and Brexit secretary David Davis.
"The direct consequences of that will be Prime Minister Corbyn".
It comes as federal minister Christopher Pyne reassured the United Kingdom that Australia will have a good relationship with the country's new foreign secretary Jeremy Hunt following Boris Johnson's resignation.
May must now move quickly to try to win the EU's support for her Brexit proposal to unblock talks.
She told BBC Two's Newsnight: "I think if the Prime Minister makes further concessions with the European Union then there will no doubt be more resignations from Brexiteers in the Cabinet, from junior ministers to PPSs because there is only so much that you can give in a negotiation".
Widdecombe, well-known in Britain as being characteristically blunt, served in government under Prime Minister John Major, and in opposition under William Hague, where she was frequently tipped as a future party leader. On Tuesday, two more lawmakers followed them out the door.
In 1982, three foreign office ministers quit, taking responsibility for Argentina's invasion of the Falkland Islands.
But her administration was thrown into disarray within 48 hours, as first Mr Davis and then Mr Johnson said that they could not commit themselves to promote the plans under the doctrine of collective responsibility.
The Guardian newspaper quoted an unnamed Conservative MP saying the resignations would continue in protest against her plan to keep strong economic ties with the European Union - dubbed the Chequers plan after her country retreat where it was agreed last week.
"I can only regret that the idea of Brexit has not left with Davis and Johnson". "Very supportive. I maybe will speak to him when I get over there".
The British leader may have stilled the waters over a possible leadership contest, but some Conservative Brexit supporters are still incensed over what they see as her decision to break her promise for a clean break with the EU.
Johnson spoke for angry Conservative Brexit-backers in his resignation letter to May when he complained that voters weren't going to get the things he'd promised them when he campaigned to leave the EU.
May's personal authority was badly damaged after she called a snap election past year to strengthen her hand in Brexit talks but instead she lost her parliamentary majority, meaning she has to rely on a small Northern Irish party to govern. He said: "Now that the secretary of state has resigned, clearly there will be more scrutiny on the deal".
But it soon began to unravel when Davis resigned late on Sunday and launched a no-holds-barred attack on her plan, calling it "dangerous" and one which would give "too much away, too easily" to European Union negotiators, who would simply ask for more.
The Sun, Britain's biggest-selling newspaper, said there had been "blunder after blunder" by May. "Now there is chaos", it said in its editorial. A "responsible government" has to prepare for a variety of outcomes in the negotiations, "including a no deal".
While May is certainly in a precarious situation, the absence of banner-barer leading the charge for a clear and widely supported alternative position to the Chequers deal makes her relatively safe for now. "It's also what he says about Justin Trudeau ('good relationship"), Angela Merkel ('really great relationship"), Mitch McConnell ('relationship is very good') and even Barack Obama ('very good relationship').
By the time the Cabinet members emerged from their country house retreat, it looked like May had managed to combine option one with a large helping of fudge, which seemed to be quite a coup for a prime minister not used to success.