The Conservative grandee criticized the “brazen excuses” about the events in Downing Street and said Mr Johnson must go if he deliberately lied to Parliament.
The Prime Minister is expected to be among the more than 50 individuals in No 10 and Whitehall who will receive legal questionnaires from officers working on Operation Hillman.
But he deflected questions about whether he will quit if Scotland Yard issues him with a fixed penalty notice over any possible breach of coronavirus regulations.
In a scathing speech at the Institute for Government in London, Sir John said “deliberate lies to Parliament have been fatal to political careers” and “must always be so”.
“At No 10, the Prime Minister and officials broke lockdown laws,” he said.
“Brazen excuses were dreamed up. Day after day the public was asked to believe the unbelievable. Ministers were sent out to defend the indefensible – making themselves look gullible or foolish.
“Collectively, this has made the Government look distinctly shifty, which has consequences that go far beyond political unpopularity. No Government can function properly if its every word is treated with suspicion.”
Sir John, a longstanding critic of Mr Johnson, said trust in politics has hit a “low ebb, eroded by foolish behaviour” while “too often, ministers have been evasive, and the truth has been optional”.
The Prime Minister has already resisted calls to resign, but these are expected to grow louder if he is issued with a fixed penalty notice.
Asked at a press conference with Nato secretary-general Jens Stoltenberg to discuss Russian aggression against Ukraine, the Prime Minister said he would not outline how he will respond until the police investigation concludes.
“That process must be completed and I’m looking forward to it being completed and that’s the time to say more on that,” he told reporters in Brussels.
Pressed a second time, Mr Johnson responded: “I understand but we’re going to wait for the process to be completed.”
Further Conservative MPs are poised to call for a vote of no confidence in the Prime Minister if he is fined, or further damaging details emerge from the Sue Gray inquiry.
Scotland Yard said it will be dispatching the questionnaires by the end of the week as officers consider whether to widen the investigation to cover a Christmas quiz in No 10 in December 2020.
Police are reconsidering their decision not to include that event after a photograph emerged of Mr Johnson and colleagues near an open bottle of sparkling wine.
Adam Wagner, a lawyer who has been studying Covid-19 regulations, described the dispatching of questionnaires as “very significant” because it means the police think they are approaching a point where they can start issuing ends.
The human rights barrister told BBC Radio 4’s Today programme: “It sounds to me, although I haven’t seen the letters, that they’ve decided that relevant gatherings were potentially a breach of the regulations and now they’re asking people ‘Did you have some sort of reasonable excuse?’, which, in law, would effectively be a defense for being there.”
Mr Wagner said a fixed penalty notice is the most likely punishment that would be issued by police as they investigate 12 gatherings.
With Mr Johnson alleged to have been at up to six of them, the lawyer suggested breaches would tot up cumulatively so the Prime Minister “could still be in line for over £10,000 worth of fixed penalty notices if they accumulate”.
Defense Secretary Ben Wallace was unclear about whether Mr Johnson will tell the public if he receives a police questionnaire.
“The Prime Minister has said he will be full and transparent. He will notify if he is receiving any form of fine etc but he’s also said he will publish the Sue Gray report in full,” he told Today.
The Cabinet minister said more damaging photos of events could be leaked in the coming days.
“Yes, there could be a photograph tomorrow, the next day or the day after – that’s clearly what’s behind some of the people’s motives,” he told Times Radio.
The Metropolitan Police said the questionnaire will ask for “an account and explanation of the recipient’s participation” in an event which is the subject of police inquiries.
Recipients will be advised that the questionnaire has “formal legal status” and that they are required to respond “truthfully” within seven days.
In most cases the contact will be by email.
“If, following an investigation, officers believe it is appropriate because the Covid regulations have been breached without a reasonable excuse, a fixed penalty notice will normally be issued,” the statement said.
“We understand the interest in and impact of this case, and are progressing the investigation at pace.
“We are committed to completing our investigations proportionately, fairly and impartially.”
An interim report last week by senior official Ms Gray disclosed that police are investigating 12 different events at No 10 and Whitehall over the course of 2020 and 2021 for possible breaches of Covid rules.
They include the notorious “bring your own booze” event in the Downing Street garden in May 2020 attended by Mr Johnson, and a gathering in the Prime Minister’s official flat in November 2020.
The Met said the Operation Hillman team are continuing to examine more than 500 documents and 300 images provided to them by the Cabinet Office and will be seeking further information to assist their inquiry.