There were questions about his rapid, unprecedented rise. He won the presidency with Khomeini's support - the first cleric in the post - and was a surprise choice as Khomeini's successor, given that he lacked both Khomeini's popular appeal and superior clerical credentials.
His ties to the powerful Guards paid off in 2009. That year, the force crushed protests after President Mahmoud Ahmadinejad won re-election amid opposition accusations of vote fraud.
He also presided over a vast financial empire through Setad, an organization founded by Khomeini but expanded hugely under Khamenei, with assets worth tens of billions of dollars.
Khamenei expanded Iranian influence in the region, empowering Shi'ite militias in Iraq and Lebanon, and propping up then-President Bashar al-Assad by deploying thousands of soldiers to Syria.
He spent billions over four decades on these allies -- the "Axis of Resistance," which also included Hamas, the Palestinian Islamist group, and Yemen's Houthis -- to oppose Israeli and U.S. power in the Middle East.
But in 2024, Khamenei saw these alliances unravel, and Iran's regional influence shrivel, with the ousting of Assad and a series of defeats inflicted by Israel on Hezbollah in Lebanon and on Hamas in Gaza, including the killing of their leaders.
Under Khamenei's rule, Iran and Israel fought a shadow war for years, with Israel assassinating Tehran's nuclear scientists and Revolutionary Guard commanders.
It exploded into the open during Israel's war on Hamas in Gaza from 2023. In April 2024, Iran fired hundreds of missiles and drones at Israel after it bombed Tehran's embassy compound in Damascus. Israel struck Iranian soil in response.
But that was only a prelude to June 2025, when Israel's military unleashed hundreds of fighter jets to strike Iranian nuclear and military targets as well as senior personnel. The surprise attack provoked a barrage of missiles in both directions, transforming simmering conflict into all-out war. The U.S. joined the air offensive on Iran, which lasted 12 days.
The U.S. and Israel had warned they would strike again if Iran pressed ahead with its nuclear and ballistic missile programs, and, on Saturday, they launched the most ambitious attack on Iranian targets in decades.
Negotiations between U.S. and Iranian officials took place as recently as Thursday, but senior U.S. officials said that Iran had not been willing to give up its ability to enrich uranium, which the Iranians argued they wanted for nuclear energy but U.S. officials said would enable the country to build a nuclear bomb.
On the diplomatic front, Khamenei rejected any normalisation of ties with the United States. He argued that Washington had backed hardline groups like the Islamic State to inflame a sectarian war in the region.
Like all Iranian officials, Khamenei denied any intent to develop nuclear weapons and went so far as to issue an Islamic ruling, or fatwa, in the mid-1990s on "production and usage" of nuclear weapons, saying: "It is against our Islamic thoughts."
He also supported a fatwa issued by Khomeini in 1989, which called on Muslims to kill the Indian-born author Salman Rushdie after the publication of his novel "The Satanic Verses."
Khamenei's official website confirmed the ongoing validity of the death edict as recently as 2017. Five years later, Rushdie was stabbed while giving a public lecture in New York. The writer was gravely wounded but survived. The perpetrator, who was sentenced to 25 years in prison in 2025 for attempted murder, did not testify at the trial.
The late ayatollah leaves an Islamic Republic wrestling with uncertainty amid the attacks from Israel and the United States, as well as growing dissent at home, especially among younger generations.
"I just want to live a peaceful, normal life ... Instead, they (the rulers) insist on a nuclear program, supporting armed groups in the region, and maintaining hostility toward the United States," Mina, 25, told Reuters by phone from Kuhdasht in the western Lorestan province at the start of 2026.
"Those policies may have made sense in 1979, but not today," the jobless university graduate added. "The world has changed."