The political veteran ranted about the Conservative party not having an agreed negotiating position with the EU for the Brexit talks before the programme’s host took him to task on the issue.
Bored of the politician’s rhetoric Mr Dimbleby interjected: “Does Labour know what it wants to do?”
The simple question from the presenter caused the audience to burst into laughter as the hypocritical nature of Mr Prescott’s argument was exposed.
Labour has flip-flopped on its Brexit position with different members of the shadow cabinet claiming the political party has different stances.
The policy decision expressed by the Labour front-bench range from remaining a part of the single market to completely leaving the customs union.
Struggling to contain herself after Mr Dimbleby’s question, Ms Tominey replied that Labour had “no idea” what it wanted from Brexit.
The intervention by the Sunday Express journalist clearly infuriated the former Deputy PM.
Unable to let the comment go he angrily retorted: “Have you got a problem?”
He then went to continue his point before his fellow panelist said: “No, I’m just saying Labour doesn’t know what it wants to do.”
Mr Prescott was clearly not expecting his question to be answered by Ms Tominey and looked furious at her response.
In a desperate attempt to get the final say in the argument Mr Prescott once again responded.
He pathetically said: “Are you saying that or should I explain it?
“You’ve come to an opinion before you hear me.
“That’s the Sunday Express for you.”
In another part of the programme, the ex-MP was also the subject of laughter from the Question Time audience.
He said: “I fought in the 1975 election to keep out of the EU, or the common market as it was then because it was either going to be the United States of Europe or a state which I didn’t believe in.
“In the last one, I fought to remain and stay in and I lost.
“And that is one of the difficulties.”
As Tony Blair’s old number two made his confession the audience, and some members of the panel, howled with laughter.