The Treasury’s annual report and accounts for 2022-23 showed the two former prime ministers both received – and kept – payments of £18,600.
Ms Truss was in office for just seven weeks before Tory MPs turned on her and forced her out of No10 last autumn, as they had done with Mr Johnson a few months earlier.
Ms Truss’s first choice as Chancellor, Kwasi Kwarteng, automatically received £16,876 after overseeing six weeks of unprecedented economic turmoil before being sacked.
Rishi Sunak also received £16,786 after quitting as Chancellor last July in protest at Mr Johnson’s conduct as PM, but the report noted Mr Sunak repaid the amount in full.
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With a raft of resignations and sackings during last year’s turmoil, the automatic severance payments to former ministers totalled £455,392.
Similar payments are given to Holyrood ministers, based on their salaries.
Much of the money went to ministers who quit or were sacked under Mr Johnson, but then rejoined Mr Sunak’s administration a few months later.
Grant Shapps received £16,876 when Ms Truss replaced him as Transport Secretary last September but is now back in government. He reportedly gave half of his cash to charity.
Michael Gove also received £16,876 when he was sacked by Mr Johnson as Levelling Up Secretary, a role he has returned to under Mr Sunak.
Both his successors – Greg Clark and Truss appointee Sir Simon Clarke – also received £16,876 on leaving the department.
Among those also benefiting was Chris Pincher, who quit as deputy chief whip over allegations he groped two men while drunk in the Carlton Club. He got £7,920.
Mr Johnson’s mishandling of the episode precipitated the crisis that led to his downfall.
The Commons Standards Committee recently recommended Mr Pincher be suspended from the House for eight weeks after upholding the allegations against him.
The Tamworth MP could appeal against the findings, but the summer recess means even if he does not, MPs will not be able to approve his suspension until September.
The Treasury report also showed its top civil servant, Sir Tom Scholar, received £457,000 in severance and other payments after he was controversially sacked under Ms Truss.
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His enforced exit contributed to worries about the Government’s economic plans and the negative market reaction to Mr Kwarteng’s mini-budget.
Labour deputy leader Angela Rayner said: “After the mess the Tories have left our country in, they should be hanging their heads in embarrassment, not walking away with an enormous payoff.
“When people up and down the country are struggling to pay their mortgages and put food on the table, it shows a staggering lack of shame for them to accept this money, but is exactly what we’ve come to expect from a bunch of Tories who only care about themselves.”
Liberal Democrat deputy Daisy Cooper said: “This is a slap in the face for all those who have seen their mortgages soar because of Truss and Kwarteng’s disastrous mini-budget.
“It is frankly insulting that whilst people struggle with the cost-of-living crisis, those responsible for their financial hardship are being showered with tens of thousands of pounds of taxpayers’ cash.
“If any of these disgraced former Conservative ministers had a shred of integrity left they would hand these payouts back.”
Ministers are entitled to severance payments worth a quarter of their ministerial salary on leaving office if they are aged under 65 and are not reappointed within three weeks.
The Prime Minister’s official spokesman said: “Obviously, there are laws that need to be followed at all times when coming up with agreements on severance pay.”