The new murals - mainly painted in white, red and blue, the colours of the US flag - were unveiled by Major General Hossein Salami, the head of Iran's Revolutionary Guards, at the former mission turned museum.
One of them showed a crumbling Statue of Liberty, its right torch-bearing arm having broken off.
Another depicted the triangle of the Eye of Providence, the symbol used on the back of the US dollar bill, in a sea of blood in which skulls are floating.
A third showed the American Global Hawk drone that was shot down by Iran in June over the Strait of Hormuz, with bats flying out of it.
Next to it another work showed an Iran Air plane that was shot down by an American warship over the Gulf on July 3, 1988, with white doves flying out of it.
290 people were killed in the tragedy which Washington has called a "mistake" and for which Iran has for years demanded an apology.
During his speech, General Salami reiterated Iran's grievances against the US.
He accused it of being the only country to have used nuclear weapons, twice in Japan in 1945, and yet of blocking other countries, especially Iran, from benefitting from a civil nuclear programme. He also charged that Washington is lying when it claims to support human rights and democracy, arguing that it backs nearly "all dictators" on Earth. Tehran is preparing to mark on Monday the 40th anniversary of the hostage crisis, an act that continues to poison Iran-US relations.