The images, mainly painted in the colors of the US flag, were put on display during a ceremony attended by Major General Hossein Salami, the chief commander of the Islamic Revolution Guards Corps (IRGC).
One of the 16 murals showed a crumbling Statue of Liberty, its right torch-bearing arm having broken off. Another depicted a revolver with a stars and stripes pattern, but with its barrel drooping downward and a bullet falling out.
A third painting featured Iran's downing of an American Global Hawk drone, illustrated with bats flying out of it.
A fourth showed the triangle of the Eye of Providence in a sea of blood full of floating skulls. A fifth image glorified a soccer goal Iran scored against the US in the 1998 World Cup.
A sixth work showed an Iran Air passenger plane that was shot down by an American warship over the Persian Gulf on July 3, 1988, with white doves flying out of it.
As many as 290 people were killed in the criminal act which Washington called a "mistake” and for which Iran has been demanding an apology ever since.
A seventh drawing depicted the Great Seal of the United States, with the eagle holding bullets and drug needles in its claws.
Saber Sheikh-Rezaei, the murals' designer, said the new images share the old political message but are fresher in technique and reflect more recent events.
"Many of the original works conveyed an old and dilapidated picture of Tehran and the Iranian people, but the works shown today ... will have a fresh visual language for at least the next 10 to 15 years," he told AFP.
General Salami reiterated Iran’s grievances against the US, saying the United States is the only country to have used nuclear weapons, twice in Japan in 1945, and yet is blocking other countries, especially Iran, from benefiting from a civil nuclear program.
He also said Washington is lying when it claims to support human rights and democracy, adding it backs nearly "all dictators” on Earth.
The United States, General Salami said, has for decades been stuck in "a downward spiral" and its decades-long failure to score a political victory proves that the global resistance front is growing.
Iranians are expected to hold nationwide rallies on Monday to commemorate the anniversary of the former US embassy's takeover.
On November 4, 1979, a group of university students took over the embassy, which they believed had turned into a center of espionage, plotting to overthrow the nascent Islamic Republic, and held 52 American diplomats for 444 days.
Documents found at the political mission corroborated claims by the revolutionary students that Washington had been using the compound to hatch plots against Iran.
November 4, which falls on the 13th day of the Iranian calendar month of Aban, is also known as the Student Day and the National Day of the Fight against Global Arrogance.
Anger toward America had already been growing throughout 1979 as Iran’s revolutionary government took hold, but it boiled over in October when the United States took in the ailing shah for medical treatment.
Many of those sentiments remain today amid the escalating tensions between Tehran and Washington, following the US withdrawal from the 2015 nuclear deal and subsequent sanctions that have hit ordinary Iranians hard.
Outside the former embassy’s shaded red brick walls, former protester Hossein Kouhi said he had turned out in 1979 to denounce what he called US intervention in Iran’s internal affairs, something he says continues today.
"I had a good feeling then, but we have had a bad fate,” said Kouhi, now 76, as he blamed the US for shortages of medicine in Iran because of the sanctions.
"Even today, if we allow, it (the US) will come here to plunder Iran, just like it’s doing to other countries in the region. No foreigner is a friend of Iran. They all lie,” he told the Associated Press.
Zahra Tashakori, a 41-year-old schoolteacher, agreed, saying she was glad the American presence was long gone.
"Look at their movies. They promote violence and other bad things in the societies,” she said. "They ruined wherever they intervened in the region. Just look at Iraq, Afghanistan and Syria.”
The Trump administration insists upon continuing its "maximum pressure” campaign against Iran.