It was a fresh declaration by the 5-4 majority that many limits on big-money contributions violate the givers' constitutional free-speech rights, continuing a steady erosion of the restrictions under Chief Justice John Roberts. The biggest of those rulings was the 2010 decision in the Citizens United case that lifted restrictions on independent spending by corporations and labor unions.
Wednesday's ruling voided the overall federal limit on individuals' contributions - $123,200 in 2013 and 2014 - and may have more symbolic than substantive importance in a world in which millions in unlimited donations from liberal and conservative spenders already are playing a major role in campaigns.
The ruling will allow the wealthiest contributors to pour millions of dollars into candidate and party coffers, although those contributions will be subject to disclosure under federal law, unlike much of the big money that independent groups spend on attack ads.
The early beneficiaries could be the political parties, which have lost influence amid the rise of independent spending, and challengers who may have been cut off from getting money from wealthy contributors who previously hit the cap that the court invalidated Wednesday.
Roberts said the aggregate limits do not act to prevent corruption or the appearance of corruption, the rationales the court has upheld as justifying contribution limits.
The overall limits "intrude without justification on a citizen's ability to exercise 'the most fundamental First Amendment activities'," Roberts said, quoting from the court's seminal 1976 campaign finance ruling in Buckley v. Valeo. By contrast, Roberts said the individual or "base limits remain the primary means of regulating campaign contributions."
The justices left in place limits on individual contributions to each candidate for president or Congress, now $2,600 for a primary and another $2,600 for the general election.
Justice Clarence Thomas supported the outcome, but said he would have wiped away all contribution limits as violating the First Amendment.
Justice Stephen Breyer, writing for the liberal dissenters, said that the court's conservatives had "eviscerated our nation's campaign finance laws" through Wednesday's ruling and the earlier Citizens United case.
"If the court in Citizens United opened a door, today's decision we fear will open a floodgate," Breyer said in comments from the bench. "It understates the importance of protecting the political integrity of our governmental institution. It creates, we think, a loophole that will allow a single individual to contribute millions of dollars to a political party or to a candidate's campaign."
Breyer adopted examples put forward by the Obama administration and campaign-limits supporters showing that an individual now will be able to make $3.6 million in contributions to candidates and parties, hand it over in one check to maximize his sway and have much or all of it directed to a favored candidate. Breyer said the money may have to be divvied up among state and national party organizations and rerouted, but that it can be done without violating the law.
Roberts said the dissenters' fears were overstated because other federal laws prohibit the circumvention of the individual limits and big donors are more likely to spend a lot of money independently in support of a favored candidate.
Running for federal political office has grown steadily more expensive, driven by the costs of advertising, travel, pollsters and the like. Most candidates pay for their campaigns with contributions from individual donors. That money is disclosed in reports filed with the Federal Election Commission.
But under the 2010 Citizens United decision, the wealthiest donors seeking outsized influence on campaigns have found a new avenue for their money. Outside groups known as super PACs or nonprofits can take unlimited contributions and spend independently to sway voters. Those donations are often undisclosed, leading critics to refer to them as "dark money."
Reaction to Wednesday's ruling generally followed party lines, with advocates of capping money in politics aligned with Democrats in opposition to the decision.
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.