The justices, by a 6-3 vote, said Missouri did not violate free-speech rights when it capped individual contributions at $1,075 for state races.
About two-thirds of the states impose campaign contribution limits.
A federal appeals court had struck down Missouri's limits, but Monday's decision reversed that ruling.
The new decision comes in an election year in which more than $3 billion is expected to be spent for candidates for federal offices, including the presidency.
The nation's highest court had not ruled on contribution limits since 1976, when in a landmark decision called Buckley vs. Valeo it said free-speech rights trump any attempt to limit an individual candidate's spending.
"The principal issues in this case are whether Buckley vs. Valeo ... is authority for state limits on contributions to state political candidates and whether the federal limits approved in Buckley, with or without adjustment for inflation, define the scope of permissible state limitations today," Justice David H. Souter wrote for the court.
"We hold Buckley to be authority for comparable state regulations, which need not be pegged to Buckley's dollars," he said.
Left unaffected by Monday's decision is currently unregulated "soft money" contributions made to groups that spend money without any ties to specific candidates.
The 1976 decision drew a distinction between spending, which it said could not be capped, and contributions, for which it upheld the current $1,000 limit on individual contributions in federal elections.
The 1976 ruling focused on a federal law enacted after the Watergate scandal of the early 1970s. The Missouri limits also $1,000 - before adjusted to $1,075 - were not imposed until 1994.
The 8th U.S. Circuit Court of Appeals ruled that Missouri's limits must fall because inflation had eroded their fairness and because state officials had not proved that larger donations would corrupt elections.
The appeals court had been told that $1,075 in today's dollars amounted to only $378 in 1976 dollars.
But Souter referred to conflicting views on the effect of large political contributions and said, "There is little reason to doubt that sometimes large contributions will work actual corruption on our political system, and no reason to question the existence of a corresponding suspicion among voters."
He was joined by Chief Justice William H. Rehnquist and Justices John Paul Stevens, Sandra Day O'Connor, Ruth Bader Ginsburg and Stephen G. Breyer.
Justices Anthony M. Kennedy, Clarence Thomas and Antonin Scalia dissented.
"The court's decision has lasting consequences for poliical speech in the course of elections, the speech upon which democracy depends," Kennedy said in a dissenting opinion.
But Stevens, confronting Kennedy's rationale in a separate opinion, said, "Money is property; it is not speech."
Writing for himself and Scalia, Thomas said, "Buckley was in error and I would overrule it. I would subject campaign contribution limits to strict scrutiny, under which Missouri's contribution limits are patently unconstitutional."
The state's limits had been challenged by Bevis Schock, a St. Louis lawyer who founded a political action committee called Shrink Missouri Government. He balked at the limits imposed on his contributions to candidates who support small government.
Schock wanted to give more than the legal limit to his friend Zev David Fredman, an unsuccessful candidate in the Republican primary for state auditor in 1998.
When the case was argued before the justices in October, they appeared deeply split.
At one point, Souter said, "Most people assume - I do certainly - that someone making an extraordinarily large contribution is going to get something extraordinary in return."
But Scalia extolled a wealthy man's right "to participate in the democratic process as fully as he is able."
In defending Missouri's law, state Attorney General Jay Nixon warned the court that ending or severely weakening contribution limits would lead most Americans "to believe that their government is literally for sale."
But D. Bruce La Pierre, a St. Louis lawyer representing the Shrink Missouri Government PAC, said, "We can try trusting the American people" to decide when political candidates are taking too much money from any one contributor.
The case is Nixon vs. Shrink Missouri Government, 98-963.