Donald Trump says he would "encourage" Russia to attack any Nato member that fails to pay its bills as part of the Western military alliance.
He said he had once told a Nato leader he would not protect a nation behind on its payments if it came under attack from Russia, and would "encourage them to do whatever they hell they want".
Members of Nato commit to defend any nation in the bloc that gets attacked.
The White House called the comments "appalling and unhinged".
Speaking during a rally in South Carolina on Saturday, Mr Trump said he had made his comments about Russia during a meeting of leaders of Nato countries.
He recalled that the leader of a "big country" had presented a hypothetical situation in which he was not meeting his financial obligations within Nato and had come under attack from Moscow.
Mr Trump said the leader had asked if the US would come to his country's aid in that scenario, which prompted him to issue a rebuke.
"I said: 'You didn't pay? You're delinquent?'... 'No I would not protect you, in fact I would encourage them to do whatever they want. You gotta pay.'"
A White House spokesman said the former president was "encouraging invasions of our closest allies by murderous regimes", and labelled the comments "appalling and unhinged".
He added that the statement "endangers American national security, global stability and our economy at home".
Mr Trump, the favourite to run again as the Republican candidate in this year's US presidential election, has long been critical of Nato and what he sees as an excessive financial burden on the United States to guarantee the defence of 30 other nations.
Russia launched its full-scale invasion of Ukraine in 2022, after Mr Trump left office. He has since bemoaned the amount of US money sent to Ukraine, which is not a Nato member.
The US has provided Ukraine with more financial support than any other country - totalling more than $44bn (£34bn) since the 2022 invasion, according to White House figures from December.
However, Republicans in Congress have since the turn of the year blocked all new funding - demanding tough measures to restrict migration into the US on its southern border, and then refusing the amended bill when it was presented earlier this week.
Mr Trump celebrated that rejection during Saturday's rally, saying the proposals made by President Biden had been "disastrous".
The two issues have now been successfully separated, meaning that senators are now able to debate the aid money separately.
BBC