In a stern rebuke to the party that came into power in 1994 with Nelson Mandela
at its helm, South Africans voted for change in large numbers.
Nationally, the party garnered 53.9% of the vote. The Democratic Alliance got almost 27% while the distant third-placed Economic Freedom Fighters' party had 8.2%.
The ANC even lost its seat in the stronghold of Nelson Mandela Bay, with all votes counted showing a victory for the opposition Democratic Alliance. Losing in key metro areas, it was also unable to unable to get a majority in the urban areas of Johannesburg and Tshwane.
The party will need to form a coalition to govern.
Across the country, the ANC has maintained a majority of support with strong showings in rural areas, but it has slipped below the key bellwether of 60% on the national stage.
At the last general election in 2014, the ANC took more than 60% of the vote.
Is Zuma a liability for ANC?
Municipal elections are not usually much of a show in South Africa, but the dramatic shift in support from the ANC to the Democratic Alliance could serve as a sign that change may come at the parliamentary and presidential levels, too.
South Africans are increasingly expressing frustration with rampant corruption and poor public services.
The ANC has stood by President Jacob Zuma despite a series of scandals, but even some within the party admit he could be a liability.
During the municipal elections almost every local government seat was up for grabs, including urban powerhouses such as Johannesburg as well as tiny municipalities.
More than 26 million people were registered to vote, and more than 61,000 competed for seats.
South Africans on Instagram posted pictures of their inked thumbs to show they cast their vote Wednesday.
South African rapper AKA posted that the vote would make the ANC "more efficient, stronger and better."
Both parties had been accused of trying to use Mandela's legacy to their advantage in the campaign.
In a colorful rally in Soweto, once an absolute lock-in for the ANC, the charismatic opposition leader Mmusi Maimane tapped into his humble roots there.
"The ANC has turned its back on everything Nelson Mandela fought for," said Maimane, a former pastor who claimed the Democratic Alliance represents Mandela's nonracial vision for South Africa better than the ANC.
The opposition's strategy has sparked fury among the ANC leadership and supporters. Mandela was, after all, the leader of the ANC and the country's first democratically elected president.
The Democratic Alliance started as a liberal white party opposing the apartheid regime from within the racist system but has expanded its support among black South Africans.
New leftist upstart
The ANC before the election said it remained the most powerful political force in the country and pointed to the strides it had made in improving the lives of South Africans.
The ANC also faces a challenge from the left, the upstart Economic Freedom Fighters, led by a savvy former ANC youth leader, Julius Malema, who was expelled from Mandela's party over accusations of "sowing discontent."
His party has tapped into a deep vein of discontent at the lack of economic transformation in the country and, with the group's trademark red berets and tactical use of the media, it has become a significant populist player.