The rail minister said the deal was "substantially worse" than staying in the EU, and it was "imperative we go back to the people and check" they still want to leave.
The news will be a huge blow to the Prime Minister as Brexit talks reach another crucial crunchpoint this week.
Mr Johnson, who originally voted Remain, said today he would vote against the deal Mrs May brings back from Brussels.
She is expected to get an agreement in the coming days after signing off a withdrawal agreement plan from her cabinet.
Jo Johnson's resignation comes just months after his own brother Boris quit as Foreign Secretary – saying he couldn't back Mrs May's plans any longer.
And within ministers his siblings Boris and Rachel had weighed in to congratulate their brother's stance.
Boris lavished praise on him, saying: "We may not have agreed about Brexit but we are united in dismay at the intellectually and politically indefensible of the UK position…
"This is not taking back control. It is a surrender of control."
And Rachel added: "Am hugely proud of my honourable and principled brother Jo who has put the interests of the country ahead of his political career."
In a brutal resignation letter today Jo Johnson said the PM’s proposed Brexit deal was “so far from what was once promised” and was "substantially worse" than staying in the EU.
And he said the best way forward was to given the public the option of remaining in the EU in a second Referendum.
He said: “To those who say that is an affront to democracy given the 2016 result, I ask this.
“Is it more democratic to rely on a three year old vote based on what an idealised Brexit might offer, or to have a vote based on what we know it does actually entail?”
He added: “Given that the reality of Brexit has turned out to be so far from what was once promised, the democratic thing to do is to give the public the final say."
And he said the current situation was providing the nation with a choice of "two deeply unattractive outcomes, vassalage and chaos" was a "failure of British statecraft on a scale unseen since the Suez crisis."
Sources said that more ministers could quit over her deal.
The resignation came just over a week after Sports Minister Tracy Crouch quit in the row over fixed odds betting terminals. Justice Minister Philip Lee quit over Brexit in June, followed by David Davis and Boris in July.
Within minutes of his move, pro-EU campaigner Heidi Allen tweeted: “Hats of to Jo Johnson, putting his country first.
“If we don’t know our future trade deal with the EU will look like, MPs shouldn’t support it.”
And Brexiteers rallied around to congratulated Mr Johnson.
Andrea Jenkyns said: "Very brave and principled of Jo Johnson to resign from his ministerial role. I am sure there will be further resignations if Number 10 continue with their plan for a watered down Brexit in which we are a rule-taker."
But some – including ex-Brexit Secretary David Davis – slapped down the need for another referendum.
And No10 said today: "The referendum in 2016 was the biggest democratic exercise in this country’s history.
"We will not under any circumstances have a second referendum. The Prime Minister thanks Jo Johnson for his work in government."
The news came in another brutal day for the PM as she tries to cobble together a Brexit agreement.
Aides warned hopes of a November deal were hanging by a thread after a fresh row with Brussels over the exit from a post-Brexit customs pact.
Meanwhile, the DUP threatened to vote down Theresa May’s entire deal in protest at the PM “breaking promises” over the so-called Northern Ireland backstop.
And Whitehall sources said it may not be possible to put a withdrawal agreement before Theresa May’s Cabinet on Tuesday.
The Prime Minister is in France and Belgium today to mark 100 years since the end of World War One.
Jenny Chapman MP, Labour’s Shadow Brexit Minister, responding to Jo Johnson’s resignation, said: “Jo Johnson is the eighteenth minister to resign from Theresa May’s government. She has lost all authority and is incapable of negotiating a Brexit deal within her own party, let alone with the EU.
“Theresa May is in office, but not in power.”
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