The top court was called to rule on the matter after lawmakers passed a law allowing the passports of Jerusalem-born US citizens to record their birthplace as "Jerusalem, Israel."
In 2002, despite opposition from then president George W. Bush, Congress passed a law obliging the US government to accept this designation upon request.
But, after lengthy deliberations, the court decided that this law "infringes on the executive's consistent decision to withhold recognition with respect to Jerusalem."
Washington and the broader international community have not recognised Jerusalem as Israel's capital and its final status is one of the thorniest issues in the Middle East peace process.
In a decision that had been keenly anticipated since a hearing on the issue in November last year, the court upheld the White House's right to ignore Congress' attempt to force the issue.
"The provision forces the president, through the secretary of state, to identify, upon request, citizens born in Jerusalem as being born in Israel when, as a matter of United States policy, neither Israel nor any other country is acknowledged as having sovereignty over Jerusalem," the court said in a ruling presented by Justice Anthony Kennedy.
