The exchange in the Gulf of Oman between the two rivals comes a month after the United States carried out strikes against three key Iranian nuclear sites during the 12-day war between Israel and the Islamic republic.
State TV said an Iranian army helicopter flew over the USS Fitzgerald on Wednesday morning after the vessel "attempted to approach the waters under the supervision" of Iran.
The destroyer issued threats of its own, the broadcaster said, but "the Iranian pilot... reiterated the warning to stay away from Iranian waters", forcing the US vessel to "give in" and alter its course.
In a video released by Iranian state TV, a destroyer is seen from what seems to be a helicopter window as the pilot calls on the vessel to "change course" and avoid approaching Iranian territorial waters.
A US defence official said the American ship "had a safe and professional interaction with an Iranian SH-3 'Sea King' helicopter while operating in international waters".
"This interaction had no impact to USS Fitzgerald's mission and any reports claiming otherwise are falsehoods", the official added.
Iranian forces have a history of confronting US forces in bodies of water off the country's southern coast.
In 2023, Tehran said it forced a US submarine to surface while crossing the strategic Strait of Hormuz -- a claim Washington denied.
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