In the course of a visit to Lichfield Cathedral on the start of the week, the King was confronted by a man who asked him about his brother's relationship with disgraced financier Epstein.
The protester inquired how long the King had been aware about his brother's association with Jeffrey Epstein, and also raised doubts about whether he had instructed the police to "conceal" for Andrew.
Amid the heckling, there were throngs of supporters and applause for the monarch, who was in Staffordshire for an event.
The Duke of York's connections with Epstein have been under renewed focus in recent weeks. The royal, who gave up his titles earlier this month, has repeatedly denied any misconduct.
"How long have you been aware about Andrew and Jeffrey Epstein? Did you request the authorities to cover up for Andrew?"
The monarch remained silent but carried on meeting fans, some of whom shouted "Long live the King". One supporter can be overheard requesting him for a embrace.
A female bystander outside the cathedral was also heard telling the protester to "go away" and to "shut up".
The scandal over Prince Andrew's connections to Jeffrey Epstein has been brought back into focus by sexual abuse claims repeated in Virginia Giuffre's posthumously-published book.
In the publication, Ms Giuffre alleges she had sexual encounters with the prince on multiple times, including one instance with Jeffrey Epstein and "eight other young girls"
Andrew, who agreed to a out-of-court agreement with the plaintiff in 2022, has consistently denied any wrongdoing. In 2019, he told a news program he did not remember meeting her "at all", and that they "never had any sort of sexual contact."
But recently, new inquiries have been raised about how he is able to finance his way of life despite not being a working royal.
The disclosure that he has only ever paid a nominal fee on his Royal Lodge has heightened the examination over his housing situation - even though he made significant contributions initially, including for renovations.
The political party said he should be summoned front of members of parliament to give evidence about his rental agreement of his residence.
But last week, the authorities refused to give MPs time to debate the prince's status or his home, despite increasing calls for investigation.
The royal household has not issued a statement on whether Prince Andrew might relocate of his home - or where he might reside.
Elara Vance is a tech journalist with over a decade of experience covering AI, cybersecurity, and emerging technologies across Europe.