His failure to single out white supremacists after an opposing protester died on Saturday in Charlottesville, Virginia, sparked anger that crossed political lines.
The subsequent silence on the issue of a man who usually gushes a torrent of opinion and criticism led critics to question his political motivation and attitude at one of the first moments of national angst during his presidency. Trump's omission was striking because Presidents are called as moral leaders to unite the nation, especially relating to bigoted, racist groups that most people believe have no place in US society.
But Trump has shown he loathes to appease critics, so no one knows what he will say when he confronts reporters after signing a trade measure targeting China Monday afternoon.
"It's his call," a White House official said, reflecting the frustration among some of the President's top aides over his decision this weekend to blame the violence on "many sides."
The controversy reflected how a President's words at a time of trauma at home or crises abroad can shape or inflame tensions and capture the public mood.
The President also opted last week to deliberately escalate a showdown with North Korea over its nuclear program, again revealing the extent to which he rejects the ceremonial conventions of the presidency.
On Saturday, Trump did hit out at an "egregious display of hatred, bigotry and violence" after a woman died when a man with reported neo-Nazi sympathies allegedly rammed protesters opposing an alt-right gathering in Virginia with a car.
But his comment that the wrongdoing was on "many sides" appeared to draw an equivalency between counter protesters and the extreme right. Offered a second chance to condemn the extremist by reporters, he demurred. Sunday, a White House official, declining to be identified by name, said "of course" Trump's condemnation "includes white supremacists, KKK, neo-Nazi and all extremist groups."
It was the second time in a few days that the President's rhetoric and bearing had come under intense scrutiny. Last week, his warning that he would rain "fire and fury" over North Korea if it continued its threats, appeared to envisage a nuclear strike and triggered alarm in Asia and confusion about his motivations.
The results from last week: Criticism among Republicans and conservative commentators was more acute and unified than it has been throughout his presidency and last year's campaign.
Vice President Mike Pence and other White House officials defending Trump over his reaction to the Charlottesville incident and his comments on North Korea, as well as surprising remarks about a "military option" in Venezuela on Friday, had a common problem.
They were called upon to explain, defend and often reshape the President's remarks after his rhetoric had crossed conventional lines.
Pence came to the President's defense during a news conference in Colombia on Sunday night, but was far more specific than his boss was the day before.
"We have no tolerance for hate and violence from white supremacists, neo-Nazis or the KKK," Pence said, calling them "dangerous fringe groups."
But Pence also came back to a familiar target -- the media -- blaming news coverage for criticism of his boss. "I will say I take issue with the fact that many in the national media spent more time criticizing the President's words than they did criticizing those who perpetrated the violence to begin with," Pence said.
Power of the presidential pulpit
The power of presidents is limited by the Constitution and political circumstances. But at times of national tragedy and political extremes, the presidency takes on ceremonial and pastoral dimensions, as the occupant of the Oval Office typically channels, and shapes, public emotion.
In such cases, presidential rhetoric can be a weapon or a salve. Sometimes presidents have summoned national resolve, like Franklin Roosevelt after Pearl Harbor or George W. Bush after the horror of September 11, 2001.
At other times, presidents have reached for poetry to comfort the country's hurting soul, like Ronald Reagan after the space shuttle Challenger disaster in 1986 or Bill Clinton after the Oklahoma City bombing in 1995.
Trump did not take either option on Saturday.
And an outpouring of criticism of his response to the events in Charlottesville, Virginia, and to a lesser extent his North Korea rhetoric, suggests that discomfort with his performance is unusually bipartisan.
The President's failure to single out white extremism was all the more notable because he's hardly been wary of doling out criticism in many other spheres. His entire political method is based on identifying enemies and going on the attack, from Jeb Bush to Rosie O'Donnell to Hillary Clinton to Mitch McConnell.
And it's not the first time that he has been slow to condemn the rhetoric of the extreme right. He equivocated before repudiating former Ku Klux Klan grand wizard David Duke during the White House race.
Trump has also not been slow to identify attacks abroad as part of a terrorist plague even while they were still unfolding. But he has yet to define Saturday's assault as an instance of white supremacist domestic terrorism.
Even some of Trump's most admiring allies said that he did not go far enough on a weekend that led some critics to suggest that he was concerned about alienating an extreme segment of his supporters.
"I think he needed to be much harsher relating to the white supremacists ... It's terrorism. You have to call that stuff out," said Anthony Scaramucci, who briefly served as White House communications director, on ABC's "This Week."
Colorado Sen. Cory Gardner led the criticism on CNN's "State of the Union."
"I think the President needs to step up today and say what it is. And call it for what it is. It's evil. It's white nationalism. It's bigotry and it's unacceptable. And if he doesn't do that then we can continue to answer the question of why."
After Trump threatened North Korea, and appeared to draw a red line based on North Korean threats, the White House was left scrambling.
North Korea did not take long to double down -- warning it could fire ballistic missiles towards the US territory of Guam -- leaving Trump in a compromised position, under fresh pressure to back up his words with action or to have them exposed as empty threats.
Trump's top aides tried to explain that dilemma away.
Secretary of State Rex Tillerson tried to reassure Americans that they should sleep safe, and that the path to dialogue was still open, even as alarmed regional experts warned of a worsening confrontation with Pyongyang. Then Defense Secretary James Mattis pulled back Trump's red line, redefining it by warning Pyongyang it "should cease any consideration of actions that would lead to the end of its regime and the destruction of its people."
But Trump's North Korea rhetoric was not the only time last week he rocked the foreign policy community.
On Friday, condemning the government of President Nicolas Maduro for human rights abuses and curtailment of political freedoms in Venezuela, Trump warned that he had military options to deal with the situation.
Trump has consistently argued that past US foreign policy approaches have failed — and promised to be more unpredictable.
But his rhetoric appears to be getting way out ahead of his administration's foreign policy process.
The question now, amid rising criticism of his approach at home and abroad, is whether Trump will hold his line.
No one who has watched his political career up to now will expect him to change.