The administration had defended the limits in arguments at the Supreme Court. "We are, in fact, disappointed with the decision that was announced today," said White House spokesman Josh Earnest.
Democratic Sen. Chuck Schumer of New York said, "This in itself is a small step, but another step on the road to ruination. It could lead to interpretations of the law that would result in the end of any fairness in the political system as we know it."
However, Republican National Committee Chairman Reince Priebus called the Supreme Court decision "an important first step toward restoring the voice of candidates and party committees and a vindication for all those who support robust, transparent political discourse."
The GOP and Senate Republican Leader Mitch McConnell of Kentucky had argued that other decisions relaxing campaign finance rules had diminished the influence of political parties.
Congress enacted the contribution limits in the wake of Watergate-era abuses to discourage big donors from trying to buy legislative votes and to restore public confidence in the campaign finance system.
Republican activist Shaun McCutcheon of Hoover, Ala., the national Republican Party and McConnell challenged the overall limits on what contributors may give in a two-year federal election cycle. The limits for the current election cycle included a separate $48,600 cap on contributions to all candidates.
McCutcheon gave the symbolically significant amount of $1,776 to 15 candidates for Congress and wanted to give the same amount to 12 others. But doing so would have put him in violation of the cap.
Under the rules that were struck down, a donor could give the maximum amount to fewer than 10 candidates before hitting the cap. The ceiling for giving to parties is higher, at $32,400 per year to a national party and $10,000 a year to a state or local party and a separate aggregate limit of $74,600. So a relative few contributions to party organizations would have been enough to reach the limit.
The decision "provides an avenue for an individual to be more directly supportive of more candidate and traditional political parties," said Bobby Burchfield, a partner at the McDermott, Will and Emery law firm who represented McConnell at the Supreme Court.
Challengers could now see more contributions because wealthy donors will no longer have to pick among candidates to support. With the limits, "traditionally it's the incumbents who have greater name recognition and greater ability to vacuum in that money," Burchfield said.
Relatively few Americans play in the big leagues of political giving. Some 644 donors contributed the maximum amount to candidates, PACs and parties in the last election cycle, according to the Center for Responsive Politics.
The justices resisted one plea from critics of the money restrictions that would have demolished all contribution limits, a call to abandon the court's practice over nearly 40 years of evaluating limits on contributions less skeptically than restrictions on spending.
The differing levels of scrutiny have allowed the court to uphold most contribution limits, because of the potential for corruption when donors make large direct donations to candidates. At the same time, the court has found that independent spending does not pose the same risk of corruption.
If the court were to drop the distinction between contributions and expenditures, even limits on contributions to individual candidates for Congress would be threatened, said Fred Wertheimer, a longtime supporter of stringent campaign finance laws.
The case is McCutcheon v. FEC, 12-536.
Associated Press writer Steve Peoples in Boston contributed to this report.
Follow Mark Sherman on Twitter at: @shermancourt