The court ruled 5-4 that individuals could give to candidates, parties and political groups without observing an overall cap of $123,200.
The ruling leaves in place limits on how much donors can give to a single candidate – currently $2,600.
The decision is the latest in a series which have loosened restrictions on US campaign finance.
Contribution limits were established by Congress in the 1970s in an attempt to restore the public’s faith in government after President Richard Nixon’s resignation in the Watergate scandal.
Chief Justice John Roberts wrote in Wednesday’s majority opinion that overall limits “intrude without justification” on first amendment rights, the clause of the US constitution that enshrines freedom of speech.
Critics say the ruling will expand even further the influence of big money in politics.
Four years ago, the Supreme Court lifted limits on political spending by nominally independent groups known as political action committees, in a case known as Citizens United.
Last year the high court removed restrictions on states with a history of race-biased voting laws, prompting activists to charge that the court was making it harder to vote in but easier to buy elections.
Wednesday’s vote split the court along its liberal and conservative wings, with Justice Stephen Breyer taking the unusual step of reading his dissent from the bench.
He wrote: “Taken together with [Citizens United], today’s decision eviscerates our nation’s campaign finance laws, leaving a remnant incapable of dealing with the grave problems of democratic legitimacy that those laws were intended to resolve.”
The case was brought by Shaun McCutcheon, a Republican and owner of the Coalmont Electrical Development Corporation in Alabama.
Before the US elections two years ago, Shaun McCutcheon made individual donations to 15 congressional candidates.
But he was unable to donate to another dozen candidates because that would have broken the overall limit.
“It’s a very important case about your right to spend your money how you choose,” Shaun McCutcheon has said.
He told the Associated Press news agency that he planned to spend several hundred thousand dollars ahead of November’s midterm elections.
During arguments, US Solicitor General Donald Verrilli Jr., argued in favor of the limit, telling the court if the limit were overturned, donors “could potentially funnel massive amounts of money to a favored candidate”.
Donald Verrilli argued without the overall limit, one donor giving the maximum allowed to every congressional candidate, political party and political action committee would exceed $3 million in contributions in a single election cycle.
But the court disagreed with the solicitor general’s warning, arguing the court could not interfere with such “free speech” beyond the direct limit on individual candidate donations.
The ruling may see an increase in political action groups, who while barred from directly co-ordinating with candidates’ campaigns, they may spend large amounts of money promoting a candidate or running negative adverts again the candidate’s opponents.
The groups are largely funded by business interests, wealthy individuals and, to a lesser extent, unions.
However, only a small portion of all current donors to political campaigns would be affected by the removal of the aggregate limit.
According to the Center for Responsive Politics, 646 people in the 2012 election cycle hit the maximum overall donation limit.
Those people gave more than $93 million directly to candidates and committees.
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