The briefing, first reported by the Wall Street Journal,
was confirmed to CNN by congressional aides who attended.
The additional payments were delivered to Iran in Swiss francs, Euros and other currencies.
It's sure to stoke more criticism from Republicans, who had already sharply denounced the $400 million transfer as "ransom."
That cash payment was made in January on the same day Iran released four American prisoners and formally implemented the nuclear deal. The money was flown in a plane to Iran on wooden pallets stacked with various currencies to resolve a dispute between the two countries stemming from a failed arms deal made before the Islamic Revolution in 1979 that toppled the Shah.
When the nuclear deal was implemented in January, the Obama administration announced that it agreed to pay $1.7 billion to settle the decades old dispute, although officials didn't say when or how the payments were made until now.
The administration has dismissed the notion that the payments amounted to a "ransom."
"We do not pay ransom," Obama said last month
. "We didn't here, and we won't in the future."
"We announced these payments in January. Many months ago," Obama added. "They were not a secret. It wasn't a secret. We were completely open with everybody about it."
Dawn Selak, a spokesperson for the Treasury Department, sounded a similar note Wednesday.
"As we announced at the beginning of this year and was widely reported at the time, the United States in January agreed to pay Iran $1.7 billion to settle a long-standing legal claim at the Hague," Selak said. "The form of those principal and interest payments -- made in non-U.S. currency, in cash -- was necessitated by the effectiveness of U.S. and international sanctions regimes over the last several years in isolating Iran from the international financial system."
House Foreign Affairs Committee Chairman Ed Royce introduced a measure Tuesday to censure the Obama administration for the payments.
Sen. Marco Rubio also introduced legislation that would prohibit those kinds of payments to Iran. The Florida Republican said the bill, "The No Ransom Payments Act," "will prevent this president or any future president from paying ransoms and ensure that American victims of Iranian terrorism are paid first, before the regime in Tehran can claim settlements."
"The Obama administration's ransom payment has become a source of bragging rights and extensive propaganda from the Iranian regime," Rubio wrote in an editorial published Wednesday in the Tampa Bay Times.
"The payments were made within hours of the hostages being released, and the plane carrying the hostages was not allowed to leave Tehran until the plane with the ransom payment arrived," the senator added. "Payments conditioned on the release of hostages are ransom payments, no matter what other dispute they are intended to settle."