But her dramatic political implosion after just 44 days in office has provided an almost immediate opportunity for the Tory MP to make a renewed bid to become Britain's first prime minister of colour.
It would be a historic landmark if the Hindu descendant of immigrants from Britain's old empire in India and East Africa were to take command of the world's fifth largest economy -- albeit one gripped by severe crisis.
But after securing the support of more than 100 Conservative MPs and then formally declaring his candidacy on Sunday, that reality came a step closer.
Standing in his way: former boss-turned-political foe Johnson -- who he spectacularly fell out with this year -- and fellow Conservative contender Penny Mordaunt, as well as another potential vote of party members.
Sunak failed in the summer leadership contest to convince the grassroots he was a better option than Truss. But having correctly predicted her economic agenda would spark economic turmoil, he may hope for more success the second time around.
However, Johnson remains a favourite of the party faithful and some members see his former finance minister as a back-stabber, making any such ballot highly fraught for Sunak.
Fabulously rich from his pre-politics career in finance, he has been mocked as out of touch with Britons struggling with decades-high inflation.
On the summer campaign trail, he wore expensive Prada loafers on a visit to a building site and faced accusations of "mansplaining" to Truss.
Video footage also emerged of a 21-year-old Sunak describing his mix of friends following his education at Winchester College, one of Britain's most exclusive private schools, and the University of Oxford.
"I have friends who are aristocrats, I have friends who are upper class, I have friends who are, you know, working class," he said, before adding: "Well, not working class."
A details-oriented policy wonk with a background in economics, Sunak, 42, is set to market himself as a stable choice at a time of crisis.
An early backer of Brexit, he took over as chancellor of the exchequer in February 2020 -- a baptism of fire for the Tory rising star as the Covid pandemic erupted.
He was forced to craft an enormous economic support package at breakneck speed, which he now insists must be paid off with sound fiscal plans.
In India, Sunak has been better known through his wife, Akshata Murty. She is the daughter of Indian tycoon Narayana Murthy, the billionaire co-founder of the information technology group Infosys.
The Sunaks met while studying in California and they have two young daughters, along with a photogenic dog.
The ex-ministers Instagram-friendly profile earned him the media nickname of "Dishy Rishi".
Until last year, he held a US Green Card -- which critics said suggested a lack of long-term loyalty to Britain.
And he has been dogged by difficult questions over Murty's failure until recently to pay UK taxes on her Infosys returns, which opinion polls suggest was viewed with deep disfavour by voters.
Sunak has also been damaged by the scandals of Johnson's tumultuous premiership.
He ended up with a police fine for breaching Covid rules, after joining a birthday gathering for the then-prime minister when he arrived early for a Downing Street meeting.
Johnson was also fined following an investigation into the "Partygate" affair.
Along with the controversy over his family fortune, the scandal sullied the reputation of the teetotal Sunak, who admits only to a fondness for Coca-Cola and sugary confectioneries.
Waiter to wealth
Sunak represents the constituency of Richmond in Yorkshire, northern England -- a safe Conservative seat he took over in 2015 from former party leader and foreign secretary William Hague, who described him as "exceptional".
Sunak swears his oath of allegiance as an MP on the Bhagavad Gita. Theresa May gave him his first job in government in January 2018, making him a junior minister for local government, parks and troubled families.
Sunak's grandparents were from Punjab in northern India and emigrated to Britain from eastern Africa in the 1960s.
They arrived with "very little", Sunak told MPs in his maiden speech in 2015.
His father was a family doctor in Southampton on the southern English coast, and his mother ran a local pharmacy -- a back story he never tired of telling on the leadership campaign trail.
Sunak waited tables in a local Indian restaurant, before progressing to Oxford and then Stanford University in California.
He insists that both his own family's experience, and that of his mega-rich wife's, are a "very Conservative" story of hard work and aspiration.
He will soon learn if the party members can be won over the second time asking.