Spokesman John Kirby maintained the payment was negotiated separately from the release, but said it was withheld until the Americans had left Iran, BBC reports.
Five Americans held in Iran were released in January in exchange for seven detained Iranians.
The timing of both incidents has prompted an outcry from Republicans, who accused the Obama administration of quid pro quo.
The White House, however, has pushed back on claims that the US paid a ransom for the release of the prisoners, saying the money was part of a longstanding financial dispute with Iran from before the 1979 Islamic Revolution.
“We were able to conclude multiple strands of diplomacy within a 24-hour period,” Mr Kirby told reporters. “We deliberately leveraged that moment.”
Mr Kirby’s comments come after the Wall Street Journal reported that the release of the cash depended on the departure in Iran of the prisoners’ plane.
The newspaper reported that US officials allegedly would not let a plane containing the cash in Geneva leave for Iran until a Swiss Air Force plane with the three of the US citizens on board left Tehran.
Mr Kirby reaffirmed the White House claim that the payment was part of $1.7bn (£1.2bn) owed to Iran in a military equipment deal made with the US-backed Shah in the 1970s.
The equipment was never delivered before the Shah was overthrown in 1979.
President Barack Obama had agreed to return the $400m (£300.8m) with $1.3bn ((£987m) in interest.
“It would have been foolish, imprudent and irresponsible for us not to try and maintain maximum leverage,” he said, according to ABC News.
“So if you’re asking me was there a connection in that regard in the end game? I’m not going to deny that.”
Illinois Senator Mark Kirk, chairman of the Senate Banking national security subcommittee, is demanding congressional hearings on the isse.
This, he said, was “the only way for the American people to fully known whether their tax dollars went directly to Iran’s terrorist Islamic Revolutionary Guard Corps”.
Republican party chairman Reince Priebus also released a statement to ABC News on the latest revelation.
“It’s time for the Obama White House to drop the charade and admit it paid a $400 million ransom to the world’s leading state sponsor of terrorism,” Mr Priebus said.