The court, in a 6-3 ruling powered by its conservative members, blocked an electoral map that had given Louisiana a second Black-majority US congressional district.
With November congressional elections looming, the decision could prompt Republican-led states to seek to redraw electoral maps in an effort to put at risk US House of Representatives seats considered safely Democratic.
The court's liberal justices, civil rights leaders, Democratic politicians and some legal experts denounced the decision as severely undermining Section 2 of the Voting Rights Act, which Congress enacted to bar electoral maps that would result in diluting the clout of minority voters.
"I love it," Trump told reporters after hearing of the decision, adding that he thinks that Republican-led states would now want to reconfigure their voting maps.
Section 2 had gained greater significance as a bulwark against racial discrimination in voting after the Supreme Court in 2013 gutted a different part of the Voting Rights Act. Black voters tend to support Democratic candidates.
"This is a devastating and profound step backwards for American Democracy," Democratic senator Raphael Warnock wrote on social media.
Wednesday's ruling was authored by Justice Samuel Alito and joined by his five fellow conservative justices. The three liberal justices dissented.
The ruling was issued amid a battle unfolding in Republican-governed and Democratic-led states around the country involving the redrawing of electoral maps to change the composition of US House districts for partisan advantage ahead of the November elections.
The full impact of the ruling on the US midterms was not immediately clear, though legal experts said states may try to enact new maps. Louisiana, where Black people make up roughly a third of the population, has six US House districts. Louisiana has a primary election set for May 16.
Section 2 was amended by Congress in 1982 to prohibit electoral maps that would result in undermining the clout of minority voters, even absent direct proof of racist intent.
For more than four decades, plaintiffs could win a Section 2 claim by showing that a voting map had a racially discriminatory impact under this legal standard, known as the "results test."
Wednesday's ruling, however, effectively turned Section 2 into an "intent test," experts said.
Alito wrote that the focus of Section 2 must now be to enforce the Constitution's prohibition on intentional racial discrimination under the 15th Amendment.
"Only when understood this way does (Section 2) of the Voting Rights Act properly fit within Congress's 15th Amendment enforcement power," he wrote.
The 15th Amendment, ratified in 1870 following the US Civil War that ended slavery, authorises Congress to pass laws ensuring that the right to vote not be denied "on account of race, colour or previous condition of servitude."
Interpreting Section 2 to "outlaw a map solely because it fails to provide a sufficient number of majority-minority districts would create a right that the amendment does not protect," Alito added.
In a social media post, Trump praised Alito as "brilliant" and called the ruling "a BIG WIN for Equal Protection under the Law, as it returns the Voting Rights Act to its Original Intent, which was to protect against intentional Racial Discrimination."
Democratic former president Barack Obama said the ruling frees state legislatures to reconfigure electoral districts to "systematically dilute and weaken the voting power of racial minorities - so long as they do it under the guise of 'partisanship' rather than explicit 'racial bias.'"
Justice Elena Kagan, in a dissent joined by the two other liberal justices, said the ruling rendered the Voting Rights Act "all but a dead letter," and predicted "grave" consequences.
