The dramatic scenes occurred on the third day of her evidence to the Horizon IT scandal inquiry, during which the ex-chief executive apologised to a leading campaigner - who was accused of stealing £36,000 - for being rude to her.
Subpostmasters in the public gallery at the London hearing groaned when Ms Vennells said she did not remember whether she took the advice of a public relations expert not to review five to 10 years' worth of past prosecutions.
Ms Vennells, who ran the organisation from 2012 to 2019, said during her evidence there were no words that would make the "sorrow and what people have gone through any better".
And she admitted she had no one to blame but herself for what happened.
More than 700 subpostmasters were prosecuted by the Post Office and given criminal convictions between 1999 and 2015 when Fujitsu's faulty Horizon IT system made it appear as though money was going missing at their branches.
When the BBC's The One Show featured subpostmasters fighting to clear their names in 2014, Ms Vennells told colleagues she was "more bored than outraged" at hearing about their cases, the inquiry was told, prompting boos.
An email from December 2014 was revealed in which the former chief executive claimed former subpostmistress and leading campaigner Jo Hamilton "lacked passion and admitted false accounting on TV".
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Ambitious Everton look for upgrade on the Dyche grind
Sean Dyche was never the manager Everton really wanted.
Everton ease to FA Cup win as team reboot starts
They are not used to cheering the men in the technical area.
THE ART OF NOISE
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As the thoroughly decent (and rather smart) Kasim is ejected from 'The Traitors', Helen Coffey asks whether intelligence has become a hindrance that should be concealed at all costs
The woman who cried wolf and fuelled a local race war
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Every living American president filed into pews at the Washington National Cathedral yesterday to honour one of their own at the funeral for Jimmy Carter, who died late last month at 100 years old.
Wake up and smell the fires
We live in a 'magic bubble' of denial but the LA infernos and Covid before it demonstrate why we must be better prepared
