"I highly appreciate the graciousness of the fearless Iranian people and respected officials over the past 67 months", Zarif wrote in the statement, which was posted to his verified Instagram account.
He gave no specific reasons for his decision, but cited an "inability to continue serving".
"Be happy and worthy", he added.
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But he was criticised by anti-Western hardliners in Iran after the U.S. pulled out of the agreement last May and reimposed sanctions on Iran.
Zarif's resignation, if accepted by Iran's relatively moderate President Hassan Rouhani, would leave the cleric without one of his main allies in pushing the Islamic Republic toward further negotiations with the West. However, according to the semi-official ISNA News Agency, Zarif was not present at any of Assad's meetings with Iran's supreme leader Ayatollah Ali Khamanei and Rouhani.
Iranian Foreign Minister Mohammad Javad Zarif speaks to the media in Tbilisi, Georgia, April 18, 2017.
President Donald Trump's policies have put major pressure on Rouhani's political and economic agenda, which was based on the lifting of sanctions against Tehran that are now in place again. "He offered his resignation; there was a huge outcry". Is Mr Zarif's resignation a tactic?
Hassan Mohammadi, a Tehran-based political analyst close to Rouhani, said he understood it was Zarif's third time submitting his resignation in the past year.
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Prominent members of Iran's parliament called for Rouhani not to accept the resignation.
The resignation of Iran's top diplomat was confirmed by an informed source. The International Atomic Energy Agency said in a confidential quarterly report on Friday, Feb. 22 that Iran has been abiding with key limitations set in the so-called Joint Comprehensive Plan of Action.
The U.S. has intensified its criticism of Iran under Trump, at times triggering disputes between the American commander-in-chief and Zarif on Twitter.
"The entirety of humanity is today riding in the same boat and we either sail together; or sink together", he said.
Zarif's email exchanges with Kerry at critical moments, including during the arrest of 10 US marines in Iranian waters in 2016, defused tensions between the two countries that have had no political ties since 1980.
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