Donald Trump claimed King Charles III "agrees" that Iran must never have a nuclear weapon in his State Dinner speech on Tuesday evening.
"We're doing a little Middle East work right now," Mr Trump said in his landmark address.
"Some of you might know, and we're doing very well.
"We have militarily defeated that particular opponent, and we're never going to let that opponent ever... Charles agrees with me even more than I do.
"We're never going to let that opponent have a nuclear weapon.
"They know that. And they've known it right now very powerfully."
As sovereign, the King must avoid expressing partisan views to maintain "national unity".
While not legally forbidden, expressing political opinions risks public backlash and violates the constitutional convention that the monarch must not interfere in Government policy.
Though in his own address, the King also referenced the crisis in Iran.
Charles joked about Queen Elizabeth II's first State Visit to the US - just a year after the Suez Crisis.
King Charles 'agrees that Iran must never have a nuclear weapon', Donald Trump declares
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"When my mother visited in 1957, not the least of her tasks was to help put the 'special' back into our relationship after a crisis in the Middle East," he said.
"Nearly 70 years on, it is hard to imagine anything like that happening today," he prodded.
The monarch also suggested Mr Trump should not abandon Ukraine - mere days after his youngest son attracted the President's ire for a speech in Kyiv.
"American leadership helped rebuild a shattered continent playing a decisive role as a defender of freedom in Europe," the King said.
"We - and I - shall never forget that, not least as freedom is again under attack following Russia's invasion of Ukraine."
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King Charles raising a glass to Donald and Melania Trump
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The President's bombshell Iran claim came after he raged at a new proposal from Tehran to end the war - which he started to stop it from acquiring a nuclear bomb.
Mr Trump said the Iranians had admitted their country had fallen into a "state of collapse" and was figuring out its leadership situation.
He blasted on Truth Social: "Iran has just informed us that they are in a 'State of Collapse'.
"They want us to 'Open the Hormuz Strait,' as soon as possible, as they try to figure out their leadership situation (Which I believe they will be able to do!)."
Last night, he added: "If Iran had a nuclear weapon, the whole world would be held hostage. I am doing something with Iran, right now, that other nations, or presidents, should have done long ago."
Iran's most recent offer for resolving the two-month war would shelve any discussion of its nuclear programme until the conflict was over and the chaos in the Strait of Hormuz was brought to an end.
King Charles stood outside the White House with Donald Trump
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However, US officials have warned that Mr Trump wants the nuclear issue wrapped up as his first priority.
An Iranian military spokesman told state media the Islamic Republic did not consider the war over.
Just moments after the President and King addressed the room, it emerged that Mr Trump had told his aides to prepare for an "extended blockade" of Iran, according to the Wall Street Journal.
He is said to have opted not to pursue "high risk" options - and chose to continue squeezing Tehran's economy and oil exports by preventing shipping to and from its ports.
While he was presented with further options, like resuming bombing or walking away from the conflict, he turned those down.
White House spokeswoman Anna Kelly, meanwhile, said the US has met Operation Epic Fury's military objectives - and that "thanks to the successful blockade of Iranian ports, the United States has maximum leverage over the regime".