The Metropolitan Police has now issued more than 50 fines as part of their Operation Hillman investigation into claims of lockdown-busting gatherings in Downing Street and other parts of Whitehall.
The dramatic news that Mr Johnson has been penalised will once again pile huge pressure on his position as Prime Minister.
Here, MailOnline looks at what the consequences could be:
Will Boris Johnson now have to resign over Partygate?
A defiant Mr Johnson refused to resign on the day his fine was revealed, although he issued a fresh apology for ‘the mistake that I made’.
Asked if he would quit, the PM said: ‘I want to be able to get on and deliver the mandate that I have, but also tackle the problems that the country does face right now.’
However, Mr Johnson’s political opponents are unlikely to end their calls for him to go over Partygate.
By convention, government ministers found to have misled parliament are expected to resign.
Opposition parties have claimed that Mr Johnson is already guilty of misleading the House after he previously told MPs that Covid guidance ‘was followed and the rules were followed at all times’ in Downing Street.
Boris Johnson and Rishi Sunakare both to be fined for breaching Covid rules as part of a Met Police investigation into the Partygate scandal
Scotland Yard have been investigating reports of lockdown-busting gatherings in Downing Street and other parts of Whitehall as part of Operation Hillman
Could the PM be forced out?
Mr Johnson’s fate could still be decided by Tory MPs.
Under Conservative rules, if at least 15% of Tory MPs submit a no-confidence letter then the party leader – in this case Mr Johnson – has to face a confidence vote over their leadership.
The figure currently equates to 54 Conservative MPs having to write to Sir Graham Brady, the chair of the Party’s powerful 1922 Committee.
It has been said that, when Mr Johnson first faced calls to resign among Tory MPs over Partygate at the beginning of this year, the number of letters received by Sir Graham reached the low-30s.
However, the actual number of letters is a closely-guarded secret and is only known by Sir Graham himself. He will only publicly comment once the 15% threshold is reached.
If Mr Johnson lost a vote of confidence, which would be secret ballot, there would be a leadership contest and the PM would be barred from standing.
However, if he won, Mr Johnson would be immune from another no-confidence vote for a year.
Gavin Barwell, a former MP who was Theresa May’s chief of staff when she survived a confidence vote in 2018, said the fate of Mr Johnson was ‘in the hands of Conservative MPs’.
‘What they decide will define their and the party’s reputation for the forseeable future,’ he added.
What about Rishi Sunak?
It has been suggested that Mr Johnson could also be forced to resign if Mr Sunak himself decides to quit after being fined.
The theory goes that should the Chancellor resign – and Mr Sunak has faced a tumultous few days during a row over his family’s finances and tax arrangements – it would place huge pressure on Mr Johnson to do the same.
But one Tory MP told MailOnline that even Mr Sunak resigning might not be enough to force the PM out.
‘I think that’s a bit priced in at the moment, so not as spectacular as it may have been,’ they said.
What exactly has the PM been fined for?
No10 revealed that Mr Johnson had been issued with a Fixed Penalty Notice (FPN) due to a gathering in the Cabinet Room in Downing Street on 19 June 2020 – which was the PM’s 56th birthday.
It has been claimed that up to 30 people attended a celebratory gathering that afternoon with picnic food from Marks & Spencer and a cake.
Mr Johnson said: ‘There was a brief gathering in the Cabinet Room shortly after 2pm lasting for less than 10 minutes, during which people I work with kindly passed on their good wishes.
‘I have to say, in all frankness, at that time it did not occur to me that this might have been a breach of the rules.
‘But, of course, the police have found otherwise and I fully respect the outcome of their investigation.
How much has the PM been fined?
Mr Johnson has already paid the FPN relating to the 19 June 2020 event, which is thought to be £50.
But Scotland Yard have said their Partygate investigation is still not complete, which leaves open the possibility of further fines being issued to both the PM and other senior figures.
Mr Johnson himself has not ruled out that possibility.
In England, people aged over 18 can be fined £100 for a first offence of breaching Covid rules, which is lowered to £50 if paid within 14 days.
A £200 fine is issued for a second offence, which doubles for each further offence up to a maximum of £6,400 per offence.
Some have suggested that Mr Johnson potentially faces fines of up to £12,300 if reports of his attendance at rule-breaking gatherings are all found to be true.
Could the PM have appealed?
Yes, he could have done.
The Met Police have said that individuals are allowed to dispute a FPN.
According to ACRO, the police body that processes FPNs, those who do not want to pay a fine, cannot pay, or disagree with any of the information within their FPN, can contest it and request a court hearing.
The relevant police force will then review an individual’s case and decide whether to withdraw the fine or proceed the matter to court.
In the case of Partygate, the Met Police has said that Scotland Yard officers may decide to pursue matters in a magistrates’ court if individuals choose to appeal.
Alternatively, once a fine is paid, police said the matter would be ‘considered closed’.
It seems unlikely that Mr Johnson would have wanted to risk having to appear in court by deciding to appeal his fine.
When was the last time a sitting PM was penalised for having broken the law?
Never. Mr Johnson has created history with his Covid fine.
Will the PM and Chancellor now have a criminal record?
According to ACRO, fines issued for Covid offences are non-recordable.
This means, whether an FPN is paid or contested, it will not be recorded on the Police National Computer, although local records may be held by the relevant force.
What parties were there?
Twelve alleged lockdown-busting parties held between 2020 and 2021 are being investigated by Scotland Yard.
They include a gathering held in the Downing Street garden, the event on Mr Johnson’s 56th birthday, parties in the PM’s Downing Street flat, a Number 10 Christmas party, and boozy leaving dos on the eve of Prince Philip’s funeral.