UK Edition
Sir Ivan Rogers could no longer be trusted and had to go, the former Conservative minister Iain Duncan Smith said on Wednesday.
The prominent pro-Brexit MP suggested Sir Ivan was right to resign as Britain's ambassador to the EU because civil servants had to "ultimately" accept that ministers make the decisions.
He told Sky News that Sir Ivan is "not God almighty", adding: "Whatever their opinion, the job of the civil servant is to deliver on the will of the British people."
His comments came after Sir Ivan's 1,400-word resignation letter to his staff leaked, revealing that he had launched a thinly-veiled attack on the "muddled thinking" in Theresa May's Government.
Mr Duncan Smith said the letter was "verging on the pompous" and was a sign of "sour grapes".
The former minister told BBC Radio 4's Today programme that civil servants are now having to "tear up the rulebook" for how they normally operate to deal with Brexit.
He said: "They are now having to accept and understand that we are leaving and that means therefore sometimes the views and the opinions of what you keep feeding back from various member states isn't actually sometimes quite relevant."
He went on: "It's well and good, absolutely right, to feed that back, but ministers have to sift that and decide ultimately no, what we are going to do is this, and we therefore have to get on and do it like this.
"If you don't agree, and I have full respect for him, then you have to go."
Mr Duncan Smith also suggested Sir Ivan had undermined his position by "going public" too often.
"This is now the second time it may actually prove that ministers may well be right to say that they weren't prepared perhaps to trust him quite the way they would have done with others," he said.
Sir Ivan announced his resignation on Tuesday after it was made clear Mrs May and her senior team had “lost confidence” in him over his “pessimistic” view of Brexit.
Government sources made clear that Sir Ivan had “jumped before he was pushed” and that Number 10 believed his negative view of Brexit meant that he could not lead the negotiations after the Prime Minister triggers Article 50.
But in his resignation letter Sir Ivan called on his staff to challenge "ill-founded arguments" and said that "serious multilateral negotiating experience is in short supply in Whitehall".
The implicit criticism of Mrs May will infuriate Downing Street.
Sir Simon Fraser, the former head of the Diplomatic Service who worked with Sir Ivan for "many years", warned that Britain was losing one of its biggest experts on Europe months before "very complex" Brexit negotiations begin.
He told BBC Radio 4's Today programme: "He is a highly intelligent, knowledgeable and experienced official and one of the greatest experts, if I can use the expert word, that we have on European matters in the British Civil Service."