The repayment, which settles a suit brought under an international legal tribunal, is separate from the tens of billions of dollars in frozen foreign accounts that Iran can now access after the end of nuclear sanctions.
But the timing of the announcement, one day after the implementation of the Iran nuclear accord, will be seen as pointing to a broader clearing of the decks between the old foes.
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"For the United States, the settlement could save us billions of dollars that could have been pursued by Iran. There was no benefit to the United States in dragging this out," he said.
Kerry said the claim was in the amount of a $400 million trust fund used by Iran to purchase military equipment from the United States prior to the break in diplomatic ties, plus $1.3 billion in interests.
Iranian-US ties broke down in 1979 after revolutionaries - angered at US support for the Iran's deposed monarch - stormed the American embassy and took hostages.
In 1981, the Iran-US Claims tribunal was established in The Hague to settle outstanding debts between the two countries, and Tehran filed a suit demanding the arms payment be returned.
Kerry described today's payment of the 35-year-old trust as a "fair settlement," but it is sure to draw the ire of those in Washington who think he had already made too many concessions to secure the nuclear deal.
"Iran will receive the balance of $400 million in the Trust Fund, as well as a roughly $1.3 billion compromise on the interest," he said, in a statement.
"Iran's recovery was fixed at a reasonable rate of interest and therefore Iran is unable to pursue a bigger tribunal award against us, preventing US taxpayers from being obligated to a larger amount of money."
Kerry went on to say all of the US claims against Iran at the tribunal had long been settled and had netted American companies and individuals $2.5 billion.
But he added there are more Iranian claims pending and that the United States would try to negotiate to resolve them.
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