Mr Johnson is expected to leave the front benches for the time being and spend some time repairing his reportedly slapdash finances, with newspaper columns and the speaking circuit likely to prove lucrative.
“He wants to go and put hay in the loft — in other words build up his bank balance so that he can afford to pay for the lifestyle that he has created,” trade envoy Lord Jonathan Marland said.
There are rumours that Mr Johnson, his wife Carrie and their two young children will establish a new base in south London, even as Mr Johnson remains an MP in London’s western commuter belt.
But the question of whether his career on the front line of British politics is really over remains open.
It is almost 50 years since an ousted prime minister returned for a second spell in office, but Mr Johnson has a history of recovering from political setbacks.
He made no secret of the fact that he saw his removal by Tory MPs in July as an unjustified rush of blood and believed he had unfinished business as prime minister.
“I'd never say never on anything with Boris Johnson — anything is possible,” said his former chief of staff Lord Edward Lister.
Mr Johnson still has an inquiry hanging over him into whether he misled MPs over the Partygate scandal that contributed to his demise, and a separate inquiry into Britain’s coronavirus response could lead to further criticism.
But supporters of Mr Johnson say Tory MPs will miss his charismatic appeal, and his successor will quickly find themselves in difficult political waters as they navigate Britain’s winter energy crisis.
If the new leader crashes and the Tories lose the next election in 2024, a Johnson comeback to revive the party from opposition is a “distinct possibility”, Lord Marland told BBC's Newsnight.
Boris Johnson's last days in office — in pictures
Mr Johnson’s predecessor, Theresa May, remained a constituency MP after leaving office in 2019 and has frequently needled the government from the back benches.
Another former Tory prime minister, Edward Heath, remained in the House of Commons for almost 30 years after leaving office, while Margaret Thatcher, John Major and David Cameron bowed out more quickly.
Mr Johnson could undoubtedly make life difficult for his successor if he chooses to intervene from the back benches, although he would have to defend his seat at the 2024 election — no sure thing if there is a large swing to Labour.
Mr Johnson said in his final major policy speech last week that “only time will tell” what kind of former prime minister he would be.
“My intention and what I certainly will do is give my full and unqualified support to whoever takes over from me … otherwise, ready to get on with life,” he said.
The twice-divorced Mr Johnson will be entitled to a regular MP’s salary of about £84,000 ($96,000) and receive security protection as a former prime minister, but is said to have complained to friends about the state of his finances.
Before becoming prime minister, Mr Johnson was paid £275,000 ($316,000) a year as a columnist for the Daily Telegraph and many expect that he will return to journalism once out of office.
A former correspondent in Brussels and editor of the Spectator magazine, Mr Johnson was also a regular public speaker and TV panellist during his earlier career.
Mrs May has earned as much as £127,000 ($146,000) for single post-prime ministerial speaking engagements, and Mr Johnson is likely to be more of a draw.
A memoir could also prove lucrative for Mr Johnson, whose earlier books on Winston Churchill, Ancient Rome and other subjects continue to bring in thousands of pounds a year in royalties.
Another suggestion floated after Mr Johnson’s resignation is that he could become a British special envoy to Ukraine, allowing him to maintain his personal friendship with the country’s President Volodymyr Zelenskyy.
And some Tory MPs have even called for Mr Johnson to become the next Secretary General of Nato when the position becomes vacant next year.