Reza Pahlavi, the son of the shah ousted by the 1979 Islamic revolution, and Maryam Rajavi, the leader of the People's Mujahedin (MEK), which is outlawed in Iran, said in separate statements that Khamenei must quit after over a week of war between Iran and Israel.
The whereabouts of Khamenei, who has led the country since 1989, are unclear after Israel refused to rule out killing him.
Opposition groups claim he is deep underground in a bunker and incommunicado except with a group of his closest aides.
"Now Khamenei must go," said Rajavi, saying that Khamenei's "unpatriotic project" had now "all gone up in smoke".
"No to appeasement, no to war and yes to regime change -- changing the religious dictatorship by the Iranian people and the Iranian resistance," she said.
Pahlavi, who is the figurehead for supporters of the ousted Iranian monarchy, said "the only sure way to achieve peace is for this regime to now end".
"As Khamenei considers how to respond from his underground bunker, I say to him: For the sake of the Iranian people, respond by stepping down," he said.
In another statement, 2023 Nobel Peace Prize winner Narges Mohammadi, who remains inside Iran on leave from a prison sentence, called Iran's government a "religious, authoritarian, and misogynistic regime".
Bur she said she strongly opposed the "devastating and ruthless war" and urged both sides to accept an "immediate ceasefire".
"I firmly believe that democracy and peace will not emerge from the dark and terrifying corridors of war and violence," she said.
The series of US strikes against Iran "devastated" its nuclear programme, Defense Secretary Pete Hegseth said Sunday, while insisting that Washington was not seeking to oust the clerical leadership.
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