Trump's use of the phrase "Arabian Gulf" rather than "Persian Gulf" particularly hit a nerve in a country with a fierce nationalistic streak.
"Everyone knew Trump's friendship was for sale to the highest bidder. We now know that his geography is too," wrote Foreign Minister Mohammad Javad Zarif on Twitter, referring to the US alliance with Iran's regional rival Saudi Arabia.
Despite pressure from the Arab Gulf monarchies, most international bodies still use "Persian Gulf" as the conventional name for the region's waterway, and many Iranians shared photos of US soldiers' medals and graves referring to the "Persian Gulf conflict" of the 1990s.
He also threatened to "terminate" the 2015 nuclear deal signed between Iran and six world powers unless Congress passed stringent new sanctions.
But as Iranians headed to their offices on Saturday -- the first day of the work week in Iran -- the reaction was often one of bemusement.
"Trump's statements are so ridiculous that it actually works in Iran's favour. Speaking about the 'Arabian Gulf' is taken very badly by people here," said Abbas, a 40-year-old banker who only gave his first name.
"The reaction of the Europeans shows that the United States is isolated, and only Saudi Arabia and Israel have supported Trump," he added.
The other signatories to the nuclear deal -- Britain, France, Germany, China and Russia -- have called for its preservation, saying that Iran is clearly sticking to its commitments.