The speech comes at a time when Washington's longstanding partnerships with the UK and Israel have endured friction over intelligence gaffes by the new administration.
"Diplomatically, the speech was inept at best and deliberately insulting at worst," said Jeff Rathke, deputy director of the Europe Program at the Center for Strategic and International Studies.
Trump's remarks Thursday, alongside his continued misrepresentation of how the alliance works and his failure to reaffirm US commitment to the group, is likely to further unsettle US allies, sowing doubt about US leadership and possibly making it harder for NATO leaders to convince their people of the need to spend more on defense.
Ivo Daalder, a former US ambassador to NATO, said that "this was a perfectly scripted event to deliver a very simple message that every president of the United States has delivered at the first possible opportunity, which is that the United States stands firmly behind its commitment to the defense of NATO."
"We signed a treaty, we uphold it. It was really easy," Daalder said. "And the fact that he didn't do it was disturbing and will take a long time to overcome in Europe."
Trump was making his first visit to the alliance in Brussels, where leaders had carefully scripted his visit, unveiling a memorial to the September 11, 2001, terrorist attacks to mark the only time NATO has invoked Article 5, which holds that all members will defend any one of them that's attacked.
The NATO-led alliance that came to the United States' aid in Afghanistan and Iraq sent more than 3,000 soldiers home in body bags.
A damaging first
Against this backdrop, the President accused NATO allies of shortchanging US taxpayers by not meeting the shared target of spending 2% of GDP on defense -- a misunderstanding of how the funding system works.
Trump also scored a damaging first, according to Nick Burns, a former US ambassador to NATO under President George W. Bush, by becoming the first president since the group's founding to fail to reaffirm the US commitment to collective defense, the principle that glues the alliance together.
"This is the first president since 1949 not to mention Article 5," Burns said. "Every president has reaffirmed collective defense and today was the day for him to do it."
Burns said he was "stunned" by the speech. "It was really disappointing," he said. "I support him on asking allies to spend more on defense. But there is a time and a place. And this wasn't it. The lecture was the wrong tone and this was the wrong time."
It could also damage the US leadership position in NATO, said Burns. The other nations "were looking for a tight embrace and they didn't get it," Burns said. "NATO looks for the US president to lead the alliance... (Trump) doesn't understand that. People now think of Angela Merkel as the leader of the West."
NATO Secretary General Jens Stoltenberg at his closing news conference after the summit defended Trump's message, which he admitted was "blunt."
Asked if he was disappointed that Trump didn't explictly express support for Article 5, he said just by dedicating the 9/11 and Article 5 display he was doing that.
Stoltenberg said there has been a clear message of support for NATO from the President, as well as Vice President Mike Pence, Secretary of State Rex Tillerson and Secretary of Defense James Mattis. Tillerson and Mattis have also recently delivered tough public messages on the need for NATO members to increase defense spending.
Changes made to accommodate Trump
NATO leaders had envisioned this summit as an introduction to the new US President, adjusting the format to make it more accommodating for Trump, changing the date, shortening the day-long proceedings -- in part by telling leaders to make speeches briefer -- and making a casual dinner the centerpiece of the gathering.
They had been put on edge by Trump's comments during the presidential campaign, when he'd derided the alliance as "obsolete." He changed course in April, declaring that it was no longer obsolete, but on Thursday he continued to raise an issue of past payments.
In Brussels, Trump charged that "many of these nations owe massive amounts of money from past years" and implied that these countries owed that money to the United States.
"This idea that countries owe money is flat-out wrong," said Rathke. Countries commit to the 2% target for defense spending -- a goal only five NATO members currently meet -- within their own countries. The money is not paid to a central fund, though Trump continues to allude to a system like that, raising questions about his ability or willingness to listen and learn.
"Anybody with NATO expertise knows that there is no such thing as 'debts' owed by NATO allies for what they haven't spent in the past," Rathke said.
Bedrock of trust
Analysts say that Trump and other presidents before him are right to press NATO members to meet their spending commitments, but they point out that what binds the alliance is trust == and the bedrock of that trust is Article 5.
Daalder, now president of the Chicago Council on Global Affairs, said Trump seems to see the alliance in transactional or economic terms, which is not the intent of NATO.
"It isn't about defense spending, it's about solidarity and security, which the defense spending enables," Daalder said.
Trump not only "ignored the bargain that is at the heart of NATO," Rathke said. "What the President did today was demand the resources without stating the commitment -- there was no carrot, it was all stick." That combination "will weaken the perception of American commitment to NATO," Rathke said.
"Every president has reaffirmed collective defense and today was the day for him to do it," he said. "The Europeans expected it and he didn't do it...that isn't how you lead an alliance. Sometimes you have to give tough love. But today was a chance to be big and Reaganesque and he didn't do it."
Daalder and other analysts point out that the President's failure to reaffirm Article 5 could also hurt his own cause by making it harder for NATO leader to increase defense spending.
"It was not a particularly good way to convince members that they should invest," Daalder said. "Particularly allies who have fought and died on the part of the United States."