The Islamic Revolutionary Guard Corps confirmed the commander of its Quds Force foreign operations arm had been killed by US forces in Baghdad, with Foreign Minister Mohammad Javad Zarif denouncing it as a "dangerous escalation".
"The Revolutionary Guards announces that the glorious commander of Islam, haj Qasem Soleimani, following a life of servitude, was martyred in an attack by America on Baghdad airport this morning," said a Guards statement read out on state television.
The channel said the attack was carried out by US helicopters.
"Two vehicles were attacked with missiles by US forces" and all 10 passengers, including Soleimani, were "martyred", Iran's ambassador to Iraq, Iraj Masjedi, told state television.
Iran's supreme leader Ayatollah Ali Khamenei warned of "severe revenge" for "the criminals who bloodied their foul hands with his blood", and vowed that "God willing, his work and his path will not be stopped".
He also declared three days of mourning.
"We are taking the necessary measures to transfer the bodies of these martyrs to the Islamic Republic of Iran which will be done as soon as possible," said Masjedi.
State television interrupted its regular programming to detail Soleimani's achievements in the region, recalling the many times he had "foiled" US plans.
Tributes pour in
A black ribbon was displayed on the screen and a photo montage was shown with images of Soleimani smiling and praying.
Soleimani was one of the most popular figures in Iran and seen as a deadly adversary by America and its allies.
President Hassan Rouhani said Iran and the "free nations of the region" would take revenge on the US for "this gruesome crime".
His death had "redoubled the determination of the nation of Iran and other free nations" to stand against the US, Rouhani said.
The Islamic republic's top security body called an emergency meeting over the killing.
The foreign ministry summoned an official from the Swiss embassy in Tehran, which represents US interests in Iran, to "strongly protest" the killing, according to ministry spokesman Abbas Mousavi.
The Guards said they and the "resistance front" would "start a new chapter as of today".
"Certainly, the fleeting rejoicing of Americans and Zionists will turn into mourning before too long," Guards spokesman Ramezan Sharif told state television.
"We were saddened to hear the news... but our determination has increased to take revenge on the murderous America and oppressor Zionists and this will certainly happen."
After the interview, Sharif broke down in tears and he and the reporter embraced.
'Terrible vengeance'
Zarif tweeted that "the US act of international terrorism, targeting and assassinating General Soleimani... is extremely dangerous and a foolish escalation".
"The US bears responsibility for all consequences of its rogue adventurism," he added.
His ministry said the US would pay for the "atrocity".
"The malice and stupidity of America's terrorist forces in assassinating General Soleimani, this hero martyr and the leader of combatting terrorism and extremism, will certainly further empower the tree of resistance in the region and the world," it said.
Zarif and his top aides held an urgent meeting in the morning to assess the situation, ministry spokesman Abbas Mousavi tweeted.
A former Guards chief said revenge would be exacted on the United States.
"Soleimani joined his martyr brothers but we will exact terrible vengeance upon America," tweeted Mohsen Rezai, who currently heads the Expediency Council, a top state body.
Tehran-based analyst Mohammad Marandi said the US has "declared war" against Iran and Iraq, and "it's best for Westerners to evacuate countries like UAE and Iraq immediately".
"It is best for all American citizens to leave the region immediately. US occupiers will be forced to leave Iraq," he said.