For nearly four decades, Iranian Supreme Leader Ayatollah Ali Khamenei has navigated internal dissent, economic crises and war, but the unprecedented strikes by Israel and the United States on Iran mark his greatest challenge yet.

What he decides next will have huge significance for Iran and the rest of the Middle East. But such is the cost of the assault his options are few. It?s a huge test for an 86-year-old in declining health with no designated successor.

The extent of the damage inflicted on Khamenei?s regime remains uncertain, but it struck at the heart of its power. The Islamic Revolutionary Guard Corps, a key military force upholding the Islamic Revolution?s ideals, suffered the loss of a string of seasoned commanders. Iran?s nuclear facilities, where near-weapons-grade uranium was being enriched, were severely damaged, and key scientists driving the program?s advancement were assassinated.

Khamenei?s regional armed proxy groups were already severely weakened by Israeli attacks, and billions spent on his regime?s nuclear program were lost in 12 days ? another economic wound at a time of sanctions and soaring inflation.

So penetrating were the Israeli strikes that Khamenei delivered his speeches during the conflict from an undisclosed location, signaling lingering concern over his safety. He was not among the hundreds of thousands attending nationwide funerals for the assassinated military commanders and nuclear scientists on Saturday.

And it was several days after the ceasefire took effect before the supreme leader delivered a defiant video message to the Iranian people.

?This president (Donald Trump) exposed that truth ? he made clear that the Americans will only be satisfied with the total surrender of Iran, and nothing less,? Khamenei said. He also, predictably, declared victory over Israel and the US ? a message that triggered a blunt response from Trump.

?Look, you?re a man of great faith, a man who?s highly respected in his country,? Trump said. ?You have to tell the truth. You got beat to hell.?

Once a nimble leader who used political and economic maneuvering to secure his regime?s survival, the aging Khamenei now governs an eroding and rigid state. With uncertainty surrounding his succession, the state of his nuclear program, and the strength of his proxy groups, he faces a critical choice: rebuild the same regime or open up in a way that could threaten his hold on power.

No surrender

Over the decades, Khamenei has confronted a relentless cascade of challenges that together have shaped his regime.

Inheriting a nation that in 1989 was wrecked and isolated by war with Iraq, he faced the daunting task of resurrecting his fractured economy and society. He had to manage internal dissent and rivalries within Iran?s complex clerical circles, confront unyielding international economic pressures, all while preserving the revolutionary ideals of sovereignty and independence.

He has enforced harsh internal repression amid waning public support, notably when women?s rights protesters demonstrated for weeks the death of a woman at the hands of the ?morality police,? and when mass protests erupted in 2009 over alleged electoral fraud.

Exiled Iranian groups established 24/7 media outlets broadcasting anti-regime propaganda and separatist groups leaked the secrets of his nuclear program. Israel?s spy agencies appear to have deeply infiltrated Iran, assassinating nuclear scientists and launching cyberattacks against Iran?s infrastructure.

But not once ? until now ? has he had the world?s strongest military strike his country, and a US president talk about his possible assassination in a social media post.

Israeli and American strikes on Iran, long-anticipated but widely doubted, marked only the second time since the 1979 Islamic Revolution that a foreign nation directly attacked the country, following Iraq?s invasion under Saddam Hussein in the 1980s.

Khamenei?s main external leverage points ? an advanced nuclear program and a network of proxy groups encircling Israel ? are now paralyzed.

Internally, Khamenei remains Iran?s most powerful figure, backed by a loyal support base and institutions built to safeguard his authority. Yet, with Iran reeling from recent attacks and Khamenei in hiding, the aging leader may intensify repression to preserve the revolution?s conservative ideals.

?Iranian doctrine was built around the projection of power in the region and the deterrence of adversaries, but the former is ebbed and the latter has failed. Set against a minimal goal ? survival ? the regime lives to fight another day, but no doubt it is weakened,? Ali Vaez, director of the Iran Project at the International Crisis Group, said.

Amidst the chaos, the Iranian regime must now address these internal and external problems, Vaez said, this requires ?more fundamental rethinking than Khamenei is likely to entertain.?

?Even if there is quiet on the military front, there must be a reckoning within the system and likely considerable finger-pointing behind the scenes. The intelligence failure has been comprehensive, upper echelons of the military have been wiped out, and Iran must still contend with deep challenges that preceded the war ? an economy in difficult straits, deep social and political discontent,? Vaez said.

Deep distrust

Facing unprecedented pressure and dwindling options, Khamenei, who previously issued a fatwa forswearing the development of nuclear weapons, might consider weaponizing Iran?s nuclear program as its best form of protection. Parliament last week signaled its intent to halt cooperation with the United Nations? nuclear watchdog.

Developing a nuclear bomb would be a major reversal in Iran?s public stance ? Israel says its offensive was aimed at stopping Iran obtaining a nuclear weapon, but Tehran has always insisted its program is peaceful.

When asked if he would consider bombing Iran again if intelligence reports conclude that Tehran could enrich uranium at concerning levels, Trump said: ?Sure, without question, absolutely.?

But Trump claimed ?the last thing? Iran is ?thinking about is a nuclear weapon.?

One possibility for Khamenei is to seize an opportunity to harness the rare unity in Iran against Israel?s strikes, for example, by introducing further reforms. In his speech, he reflected on the moment as one of collective strength.

?By God?s grace, a nation of nearly 90 million stood as one ? united in voice and purpose ? shoulder to shoulder, without any divisions in demands or intentions,? he said.

But as Vaez argued, Khamenei may have a limited appetite for a fundamental political and economic rethink. That conservatism may also preclude another option ? embracing a warming neighboring region and pursuing a new agreement with Washington.

Iran?s Arab neighbors historically saw Iran?s expansionist policies as a threat, but more recently have opted to repair ties with Tehran, and expressed a desire to cooperate to avoid costly conflict.

But Khamenei?s distrust of the West, deepened by Trump?s unilateral abrogation of a nuclear treaty in his first term and Israel?s unprecedented strikes this month ? launched two days before an Iranian delegation was due to hold a new round of talks with the US ? leaves uncertainty over how he will approach any upcoming negotiations.

In an intensifying attempt to bring Tehran back to the negotiating table, the Trump administration has discussed possibly helping Iran access as much as $30 billion to build a civilian-energy-producing nuclear program, easing sanctions, and freeing up billions of dollars in restricted Iranian funds, CNN reported this week citing four sources familiar with the matter said. Trump denied the report.

But if Trump wants a deal with Iran, his unorthodox public messaging to Khamenei, including implicitly threatening his assassination, could ultimately derail the talks, Iranian officials said.

?If President Trump is genuine about wanting a deal, he should put aside the disrespectful and unacceptable tone towards Iran?s Supreme Leader, Grand Ayatollah Khamenei, and stop hurting his millions of heartfelt followers,? Iranian Foreign Minister Abbas Araghchi posted to X on Friday.

In his latest speech, the supreme leader projected an image of unyielding resilience, signaling to the United States and Israel ? both nuclear powers ? that military action alone cannot dismantle his damaged yet still fortified, republic. But with unclear succession to his rule, and the loss of his powerful leverages, he now faces the task of guaranteeing the survival of the Islamic Republic he inherited. (CNN)

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