The last straw for the home secretary seems to have been her statement to MPs last week that she knew nothing of official targets for immigration removals-a claim that was quickly undermined by leaked correspondence suggesting that in fact both she and the prime minister did.
The furor has grown since the Guardian newspaper reported that some people who came to the United Kingdom from the Caribbean in the decades after World War II had recently been refused medical care in Britain or threatened with deportation because they could not produce paperwork proving their right to reside in the country.
But a leaked memo sent to her and former Immigration Minister Brandon Lewis past year detailed the plans to kick out another 10 per cent of illegal immigrants.
Johnson is married to Amelia Gentleman, the Guardian journalist behind the Windrush revelations that have led to calls for Rudd to resign.
She said: "Brandon Lewis's attempt to save the Home Secretary's career by hiding behind semantics is insulting for the people who have been affected by the Tories" heartless policies.
"Theresa May must face questions now given these terrible failures largely took place under her watch as Home Secretary".
Ms Rudd's downfall began on Monday when she apologised, saying: "There's absolutely no question about their right to remain and I apologise about any wrongdoing to them".
While she maintained she was unaware of such measures, there was mounting evidence that targets did exist and were known about within her department, making her position increasingly untenable.
Diane Abbott, Labour's shadow home secretary, also seized on a letter sent by Rudd to Theresa May a year ago in which she explicitly mentioned her "ambitious, but deliverable" desire to step up deportations.
Downing Street confirmed the development with a No 10 spokesman telling the BBC: "The Prime Minister has tonight accepted the resignation of the Home Secretary".
Mrs May faces a tricky task in choosing a new home secretary.
Ms Rudd has insisted she did not read the memo, but is facing a growing clamour to resign amid criticisms she either misled MPs or does not have a grip on her department.
Her reward, when Theresa May became Prime Minister, was to succeed her at the Home Office, a top job but seen by many as a poisoned chalice. In a statement posted online she said: "The architect of this crisis, Theresa May, must now step forward to give an immediate, full and honest account of how this inexcusable situation happened on her watch".
"Ms Rudd replied: "(Ms Cooper) raised that with me yesterday and I have said to her then as I repeat here I will look into that and I will come back to her with an answer to that question as soon as I can".
Mr Lewis said the difference between a specific local "target" and a national "ambition" is an "important distinction".