Appearing before MPs for more than six hours on Wednesday, Mr Cummings said ministers were too slow to act, health officials made ill-judged conclusions about the nature of the virus and a herd immunity strategy was abandoned at the last minute.
Painting a picture of chaos inside Britain’s corridors of power, he said the government "kind of collapsed" when Mr Johnson fell ill with Covid, and suggested Health Secretary Matt Hancock should be sacked for lying several times.
Early in the pandemic, he said, Mr Johnson regarded Covid-19 “as the new scare story” and he wanted England’s chief medical officer Chris Whitty to inject him with the coronavirus on live television.
“The truth is senior ministers, senior officials and senior advisers like me fell disastrously short of the standards the public have a right to expect of their government in a crisis like this,” Mr Cummings told the Science and Technology Select Committee.
“When the public needed us most, the government failed. I’d like to say to all the families of those who died unnecessarily how sorry I am for the mistakes that were made and my own mistakes at that.”
Appearing at Prime Minister’s Questions at the same time Mr Cummings was giving evidence, Mr Johnson said he was faced with no easy decisions.
“To go into a lockdown is a traumatic thing for a country. We have at every stage tried to minimise loss of life,” he said.
Mr Cummings said top officials “were literally skiing” when the UK should have been drawing up plans to curtail the spread of the disease early last year.
He made excoriating allegations of bad decisions and false assumptions within the government at the time, and said "the whole thing just seemed like an out-of-control movie".
“Like a scene from Independence Day with Jeff Goldblum saying, ‘The aliens are here and your whole plan is broken’,” he said.
“The NHS is going to be smashed in weeks and we’ve got days to act.”
The former chief adviser reserved much of his criticism for Mr Hancock, whom he said lied during government meetings on Covid-19.
“The Secretary of State for Health should have been fired for 15 or 20 things,” Mr Cummings said.
“I said to the prime minister he should have been fired; so did the Cabinet Secretary; so did many other senior people.”
He said Mr Hancock failed to honour a promise that people would be tested before they were sent into care homes to free up hospital beds to prevent wards being overwhelmed.
Mr Hancock said last year the government had thrown a "protective ring around" care homes at the beginning of the pandemic.
"Hancock told us in the Cabinet Room that people were going to be tested before they went back to care homes," Mr Cummings said.
"We only subsequently found out that that hadn't happened. Now, all the government rhetoric was we put a shield around care homes and blah blah - it's complete nonsense. Quite the opposite of putting a shield around care homes, we sent people with Covid back to care homes."
The policy of putting infected elderly patients back into care homes was was blamed for more than 25,000 people dying from the virus in care homes in Britain.
"I'm sure some people were tested," Mr Cummings said.
"But obviously many, many people who should have been tested were not tested and then went back to care homes and then infected people, and then it spread like wildfire inside the care homes."
Mr Cummings also accused Mr Hancock of saying that all patients got the treatment they needed during the first peak of the virus. Mr Cummings said that was contrary to briefings from the government's health experts, who had said some patients had not received necessary treatment.
He said Mr Hancock told ministers that the supply of personal protective equipment was under control in April, when that was not the case.
Mr Cummings, however, said the British government was not alone in failing to recognise the seriousness of the health crisis and "many, many institutions failed around the world".
He said even the most competent people in the world, such as Microsoft founder Bill Gates, would have had a “complete nightmare” if they were prime minister.
He said that Mr Johnson was "extremely let down by the system".
"Lots of people were literally skiing in the middle of February,” he said. “It wasn't until the last week of February that there was any sense of urgency."
He said there was a sense of “mounting urgency” within Downing Street during the week beginning March 9.
He recalled a top official telling him, “this country is heading for a disaster, I think we’re going to kill thousands of people”.
“I said, ‘I think you’re right, I think it’s a disaster’,” Mr Cummings said.
He revealed that before the first lockdown in March 2020, senior ministers and medical officials were pursuing a herd immunity strategy, suggesting that the "entire assumption" in Whitehall was that no vaccines would be available in 2020, while suppressing the first wave of infection would only lead to further surges later in the year.
He said it was hoped herd immunity would be achieved by September after the first wave had been and gone.
"That was the plan. I’m completely baffled why Number 10 has tried to deny that because that was the official plan," Mr Cummings said.
"Hancock himself, the chief scientific adviser and chief medical officer were all briefing senior journalists during the week of March 9 ‘this is what the official plan is’."
He said the government believed - wrongly, it turned out - that the British public would never accept strict lockdown measures.
The government denies that herd immunity through infection was ever its policy.
Mr Cummings spoke of his difficulties in getting Mr Johnson to announce new social distancing measures on March 12 last year.
He said former US President Donald Trump caused a distraction on the same day by asking Britain to join a bombing campaign in Iraq. Carrie Symonds, now the prime minister’s fiancée, was upset over newspaper stories about the couple’s dog misbehaving while ministers were trying to prepare a response to the Covid outbreak, Mr Cummings said.
"We had this completely insane situation in which part of the building was saying ‘we are going to bomb Iraq’, part of the building was arguing about whether we're going to do quarantine or not do quarantine, and the PM has his girlfriend going crackers about something completely trivial," he said.
The government "kind of collapsed when the prime minister got ill himself” with Covid-19 in April, he said.
He commended Foreign Secretary Dominic Raab for leading the government while Mr Johnson was in hospital.
"When Raab took over there was a conversation in Number 10 ... about calling a cabinet to try and find a replacement for the PM in case he died. That's how serious the situation was," he said.
"Nobody had dealt with the situation that Dominic Raab faced, literally since Churchill in World War Two. You had the crucial elements of the state gone, the prime minister on his death bed."
Mr Cummings said it was "completely terrible" the government won't hold an inquiry into the pandemic response until spring next year.
"Tens of thousands of people died who didn't need to die," he said.
"There is absolutely no excuse for delaying that, because a lot of the reasons for what happened are still in place now - look at the whole debate about variants."
Mr Cummings, 49, the strategist behind the Leave campaign in the 2016 Brexit campaign, was appointed chief adviser by Mr Johnson when he took power in July 2019.
He helped to secure a thumping election victory that December, but his frequent clashes with colleagues were said to have led to persistent tensions and he left government a year later.
The strategist was criticised for undermining the government's lockdown message early in the pandemic when he went on a lengthy cross-country journey with his family.
Mr Cummings claimed he and his wife needed childcare help from relatives after they both developed coronavirus symptoms, and that a lockdown-breaching drive during his stay in the north of England – to visit a local landmark – was to test his eyesight.
His defence rang hollow to many in Britain who had made sacrifices and endured isolation to follow the rules.
Mr Cummings said on Wednesday that he hadn’t told the whole truth, saying that was a “terrible mistake".
He said his real motivation in leaving London was his family’s safety, because there had been threats to his home in the capital.
Mr Cummings left his job in November amid a power struggle inside the prime minister’s office.