In an interview with The Sun, a British tabloid, the president announced that Theresa May's blueprint for a "soft Brexit" was a betrayal of British voters - one that, if implemented, "would probably end [Britain's] major trade relationship with the United States".
Just hours earlier at a lavish dinner to mark Trump's first visit to Britain as president, May made a direct pitch for a deal with Washington.
This has infuriated fervent Brexit supporters, who think it would limit Britain's ability to strike new trade deals around the world.
Trump came down firmly on the side of the Brexiteers, saying what May proposed would hurt the chances of a future trade deal between the UK and the United States.
But Trump declined to provide any details about the advice he provided May.
He told The Sun Mrs May's plan would affect trade "unfortunately in a negative way". May's Conservative party, and foreign minister Boris Johnson joined Mr. Davis in dramatically quitting this week in protest.
In the interview, Trump insisted that he would have negotiated the deal differently than May, and he said that he had provided the prime minister his "views on what she should do and how she should negotiate".
The agenda for Trump and May on Friday includes discussion on relations with Russian Federation, ahead of a summit in Finland on Monday between Trump and President Vladimir Putin.
It also plans to allow certain types of freedom of movement but confirms that it will not allow the type of free access to Britain that is enjoyed by European Union member states now.
As the Trumps dined with the Mays, protests in the British capital took place outside Winfield House, the residence of US Ambassador Woody Johnson. "So a lot of people don't like it", he said. The UK hopes to make progress on a post-Brexit trade relationship, although the scope for a bilateral trade deal would be limited if the UK remains aligned with European Union regulations on goods. It was agreed by her Cabinet only last Friday after two years of wrangling since Britons voted to leave the bloc in the referendum.
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Former Conservative party leader Iain Duncan Smith said he had "deep misgivings" about the white paper; veteran Brexit hardliner Bill Cash declared himself "deeply anxious;" and Andrew Bridgen, who has already sent a letter expressing no confidence in May to party authorities, said he "and many colleagues" had "grave concerns" about the path the government is now on, Politico reported.
"Well, I am not pitting one against the other", Trump said.
"The spirit of friendship and cooperation between our countries, our leaders and our people, that most special of relationships, has a long and proud history".
Outside the mansion, near Oxford to the northwest of London, a couple of thousand demonstrators lined the road and booed Trump's arrival.
Trump's intervention comes at the end of a tumultuous few days for May.
It "delivers on the instruction we delivered loud and clear from the British people to take back control", he added.
After spending the night at Winfield House Mr Trump will join the PM at a military base on Friday to observe a joint counter-terrorism exercise involving United Kingdom and U.S. special forces. He came directly from the North Atlantic Treaty Organisation summit, where he had questioned the US's commitment to the security alliance.
Mr Trump and his wife Melania arrived at Stansted airport, where he was met by the UK's worldwide trade secretary Liam Fox.
The interview posted online as Prime Minister May welcomed President Trump and the first lady at Blenheim Palace for a lavish gala dinner.