Boris Johnson, a leading supporter of Brexit who quit as foreign secretary in July, praised his brother's decision, saying they were "united in dismay" - despite their opposing views on Brexit - over May's handling of the negotiations.
The Conservative MP added that it would be a "democratic travesty" if the public did not get to have their say once again.
"It is entirely right to go back to the people and ask them to confirm their decision to leave the European Union and if they choose to do that, to give them the final say on whether we leave with the prime minister's deal or without it", he added.
"It has become increasingly clear to me that the withdrawal agreement, which is being finalised... will be a bad mistake", he wrote in a stinging resignation statement.
The UK is set to divorce the European Union on 29 March 2019, with the transition period set to end in December 2020, and Downing Street is seeking to settle the remaining five percent of the withdrawal agreement to prompt a deal-making summit later in November.
A Cabinet minister said leader of the pro-Brexit European Reform Group Jacob Rees-Mogg also supports the plan, while other Brexiteers said it could be worth exploring in more detail.
Mr Johnson said his role as transport minister had caused him concern about the impact of a no-deal outcome.
His resignation follows controversy on Thursday after Brexit Minister Dominic Raab faced ridicule over admitting that he "hadn't quite understood" how dependent the United Kingdom was on the Dover-Calais crossing for its trade.
Labour Shadow Brexit Minister Jenny Chapman said that Theresa May had "lost all authority and is incapable of negotiating a Brexit deal within her own party, let alone with the EU".
"This would not be about re-running the 2016 referendum, but about asking people whether they want to go ahead with Brexit now that we know the deal that is actually available to us". My loyalty to the party is undimmed.
The departing minister noted Brexit had divided Britain, political parties and "families too", but added: "what is now being proposed won't be anything like what was promised two years ago" during the referendum campaign.
A spokesperson for May's office said later Friday that under no circumstances would a second referendum be held.
Johnson is the 14th minister to have resigned from government since November previous year.
"My brother Boris, who led the leave campaign, is as unhappy with the Government's proposals as I am".
Johnson said this morning that other ministers are thinking hard about the Brexit and its implications.
Former BBC journalist and current University of Kent chancellor Gavin Esler said: "This - from a hugely respected minister - is an important development".
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He's tough so he gets up and he plays. "Guys like that, the only thing you can do is stuff them up by coaching them". He takes the ball to the line, he puts his body on the line, he doesn't play in a dinner suit.
Those that suffer from Celiac disease may be able to start eating gluten again thanks to an experimental vaccine. About 80 to 90 percent of those who have celiac disease also carry the immune recognition gene.
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