Speaking to US lawmakers, Kerry agreed Tehran's support for the Huthi militia was "critical" in shoring up the rebels.
Asked whether the Yemeni government collapsed because of Iran's support for the Huthi, Kerry replied: "I think it contributed to it .. Without any question whatsoever."
"But I do know that the Iranians were surprised by the events that took place and are hoping to see a national dialogue" take place," Kerry told the Senate appropriations committee, at the start of two days of intense budget hearings.
Yemen's Gulf neighbours have rejected the sidelining of the Western-backed President Abedrabbo Mansour Hadi as a "coup," while the UN Security Council has urged the militia to withdraw its forces from government institutions.
An aide to Hadi said today the embattled leader has retracted his resignation after escaping house arrest in the militia-controlled capital, Sanaa, at the weekend.
Hadi had tendered his resignation last month after the Shiite militia seized the presidential palace and besieged his residence in Sanaa.
The United States closed down its embassy in Yemen earlier this month, along with France and Britain, amid growing concerns about insecurity in the country.
The Huthis, whose power base is in the mainly Shiite northern highlands, overran Sanaa unopposed five months ago.
They have pushed their advance south and west into mainly Sunni areas, where they have met with fierce resistance from tribesmen and Yemen's powerful branch of Al-Qaeda.
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