TV footage shows Mohamed Morsi in 2010 referring to Zionists as “bloodsuckers” and “descendants of apes and pigs”.
US officials want the leader to clarify his “deeply offensive” comments, which they say run counter to Middle East peace efforts.
Egypt receives around $1.5 billion in annual US military and economic aid.
The financial support is linked to Egypt’s peace treaty with Israel, which the US considers a cornerstone of regional stability.
The controversy erupted after the Washington-based Middle East Media Research Institute (MEMRI) translated and released Arabic footage of interviews Mohamed Morsi gave in 2010, as a leader of the Muslim Brotherhood.
In the clip from Palestinian broadcaster Al-Quds TV, Mohamed Morsi referred to Jewish settlers as “occupiers of Palestine” and “warmongers”.
He called for a “military resistance in Palestine against these Zionist criminals assaulting the land of Palestine and Palestinian”.
Mohamed Morsi also denounced the Palestinian Authority, saying it was “created by the Zionists and American enemies for the sole purpose of opposing the will of the Palestinian people.”
In another interview, Mohamed Morsi urged Egyptians to “nurse our children and grandchildren on hatred”.
The US State Department said the comments should be repudiated.
“We completely reject these statements, as we do with any language that espouses religious hatred,” the department’s spokeswoman Victoria Nuland said.
“This kind of rhetoric has been used in this region for far too long. It’s counter to the goals of peace.”
The White House called the rhetoric “unacceptable in a democratic Egypt”.
“President Morsi should make clear that he respects people of all faiths,” spokesman Jay Carney told reporters.
However, both US officials also highlighted that Mohamed Morsi had shown his commitment to regional peace efforts since taking office in June last year.
The Egyptian leader helped broker a ceasefire between Israel and Hamas after violence flared up in Gaza in November.
And although he has been openly critical of Israel, Mohamed Morsi also pledged to abide by the peace treaty when he was voted into power.
“What he has been doing is supporting that peace treaty, continuing to work with us and with Israel on common goals, including in Gaza,” Victoria Nuland said.
“But we’ll also judge him by what he says.”
Egypt has been a key US ally since it signed the 1979 peace deal as part of the Camp David Accords.
But observers say fears remain that the new leadership might try to renegotiate the treaty.
“As long as peace and justice are not fulfilled for the Palestinians, then the treaty remains unfulfilled,” Mohamed Morsi told the New York Times shortly after winning the election last year.
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