The storming of the embassy in Tehran by students, months after the Islamic revolution, led to a 444-day hostage crisis and a break in diplomatic relations that continues to this day.
Protesters beat effigies of Trump with sticks in front of the former embassy compound while what appeared to be a dummy ballistic missile was put on display in a sign of defiance following new US sanctions.
"This year, Trump's anti-Iranian policies have mobilised more Iranians," Ali Shamkhani, the secretary of Iran's Supreme National Security Council.
Trump's administration has taken a tougher line with Iran, threatening to tear up an international accord on its nuclear programme.
Last month Trump refused to certify the 2015 deal between Tehran and world powers that lifted sanctions in return for limits on Iran's atomic programme, saying he could pull out "at any time".
The United States has also imposed new sanctions over the Islamic republic's ballistic missile programme.
A statement read out at Saturday's protest said Iranians "see the criminal America as their main enemy and condemn the denigrating remarks of the hated US president against the great Iranian people and the Revolutionary Guards."
Supreme leader Ayatollah Ali Khamenei urged Iranians on Thursday to never forget that "America is the enemy".
"To give in to the Americans makes them more aggressive and insolent. The only solution is to resist," he said.
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