Dominic Cummings, who quit his post in Downing Street last November, told a parliamentary committee on Wednesday that "when the public needed us most the government failed."
To date, more then 127,000 British citizens have died within 28 days of a positive Covid-19 test.
The most explosive allegation came when Cummings said on the record that he had personally heard Johnson say that he would rather see "bodies pile high" than impose more lockdowns on the public. Downing Street has repeatedly denied that any such comment was made.
Cummings' attack is all the more devastating because he was one of Johnson's closest aides since he became Prime Minister in 2019, and wielded unprecedented power and influence inside Downing Street.
The most damning section of Cummings' evidence came in his description of the events leading to the second lockdown on November 5.
Cummings explained that in order to show the Prime Minister how serious situation was, they held a meeting on September 21 where they pretended it was the end of October. They presented what the data would look like based on current modeling. According to Cummings, the evidence that the National Health
Service "was going to get smashed" again did not persuade Johnson. Cummings said that "any other competent" politician would have "behaved differently."
He said he would like to see an inquiry sooner rather than later, because "tens of thousands of people died who didn't need to die."
Throughout his evidence, Cummings was eager to paint himself as being alert to the seriousness of the pandemic in January 2020, long before others were taking it seriously.
He said senior government officials were occupied with other activities, be they professional or, in Cummings' words, "literally skiing," which meant the government was not on a "war footing" early enough.
Cummings claimed the Prime Minister believed the virus to be little more than a scare story and would say things like he wanted to have England's chief medical officer "inject him with Covid" live on air to prove it was nothing to worry about.
Central to Cummings' criticism of Johnson and his government is a lack of preparedness, leading to lockdowns being delayed and policies like herd immunity being pursued.
Cummings claimed he first told Johnson the UK needed to be put under hard lockdown measures on March 11, 2020. The first national lockdown was not imposed until March 23.
Cummings listed numerous reasons for this delay, ranging from a belief that the British public would not go along with "Wuhan-style" measures, to external distractions. These ranged from then-US President Donald Trump wanting the UK to join a bombing mission in the Middle East, to stories about Johnson's fiance, Carrie Symonds, being upset about stories in newspapers about the couple's dog. But ultimately, his main accusation was that the government was simply unprepared and the plan in place at this time was based on falsehoods.
On herd immunity, Cummings claimed the government was working on an assumption that nothing could stop the virus spreading and that vaccines would not be "relevant in 2020." He said UK Health Secretary Matt Hancock was "completely wrong" when he said on March 15, 2020, that herd immunity wasn't part of the government's plan, because "herd immunity was regarded as an unavoidable fact."
One of the biggest early failures of the UK's response to Covid-19 was in building a fit-for-purpose test-and-trace system. Cummings said this was the fault of the core of government collapsing around the time that Johnson went into hospital after falling ill with Covid.
He said that during this period, Hancock "stupidly" pledged to deliver 100,000 tests a day purely "so he could go on TV" and claim a success. He claimed that Hancock directly interfered with the testing program to help him reach his target, preventing the team to build the system properly.
Cummings also criticized the slow pace at which the UK closed its borders. He said arguments were made that shutting borders looked racist and would cripple the tourism industry. Cummings thinks this undermined the whole pandemic effort.
In an emotional moment, Cummings spoke of the failures around care homes and social care, which were hit badly amid the pandemic. He said Hancock had claimed people going back into care homes would be tested, when in reality many weren't. He also claimed that people working in care homes and social care were not given sufficient protective equipment nor tested often enough, allowing the virus to spread to the most vulnerable in society.
Later on Wednesday, Hancock and his team repudiated the criticism from Cummings. "We absolutely reject Mr. Cummings' claims about the Health Secretary," a spokesman for Hancock said in a statement, adding that Hancock and his department have "worked incredibly hard in unprecedented circumstances to protect the NHS and save lives."
"The Health Secretary will continue to work closely with the Prime Minister to deliver the vaccine rollout, tackle the risks posed by variants and support the NHS and social care sector to recover from this pandemic," the spokesman also said.
Beyond the pandemic, Cummings criticized the whole system of British politics, saying that a system that offers a choice between Johnson or the former leader of the opposition, Jeremy Corbyn "something's gone extremely, extremely, wrong."
He claimed that his resignation was "definitely related" to the fact Johnson's fiance was "trying to put people in particular jobs," building her own power base in Downing Street.
Speaking in the House of Commons later on Wednesday, Johnson defended his government's actions throughout the pandemic, accusing his opponents of looking in "the rear view mirror" while his government pressed on with its vaccination program.
A Downing Street official said they were "not going to respond to every allegation" but would continue to focus on the priorities of the nation, which is ending the pandemic. The official added that the Prime Minister believes Hancock has always told him the truth.
Critics of Cummings have questioned his legitimacy as a witness. During the period of time that his evidence concerns, he was arguably the most senior person working inside Downing Street, aside from Johnson.
He repeatedly won battles with other government officials, cementing his authority as the most important person in Johnson's inner circle. The Prime Minister had on more than one occasion called his former chief adviser a "genius" who he "loved" at private events at which CNN was present. During Cummings' time in government, he would often attend press briefings and lurk at the back, watching his subordinates at work, much to their discomfort.
Meanwhile, journalists would flock around a man who had come to be an almost mythical figure.
It's therefore extremely unlikely the views of Cummings were ignored or sidelined at the height of the pandemic.
It's also worth noting that Cummings is discredited for other reasons, most notably the time he drove his wife and child hundreds of miles across the country during a national lockdown after coming down with Covid-like symptoms.
Cummings said during the session that he moved his family out of London because he had received death threats.
No matter how stunning the words of Cummings might be to those watching, the reality is most of the country won't be as fixated as those in the Westminster bubble. And even those who did watch might note that Cummings failed to provide any actual evidence for his most serious claims. Without that evidence, the combination of his poor reputation and the success of the UK's vaccine rollout means this story is likely to blow over in days.
The leader of the official opposition, Keir Starmer, said Cummings' evidence was "the latest chapter of a story of confusion, chaos and deadly misjudgements." And while Johnson might be on course for a joyous summer of lockdown's end, there is a risk that at some point, this will play into a wider, damning retrospective of how his government failed the country in its hour of need.