The Moses Mabhiba stadium is one of six venues built for next year's finals and will host a total of seven matches at the 2010 tournament, including one of the semifinals.
The venue opened with a South African premier league match between AmaZulu and Maritzburg United.
Capacity was restricted to 22,000 with only the lower tier of the stadium used and sold out a week before the match, but rainy conditions kept thousands away, a league spokesman said.
The stadium's outstanding feature is a cable car which ascends to a viewing platform at the top of a 350m arch, which spans across one side of the stadium to the other.
Visitors are able to travel to the top of the arch above the playing surface and have panoramic views of the nearby shoreline and city.
Durban is the second of the new stadiums built for the World Cup to be opened, following Port Elizabeth in June.
Stadiums at Cape Town, Nelspruit, Polokwane and Soccer City in Johannesburg, which will host the opening match and final, are due to open by February.
Four other World Cup venues have been renovated and were used during the Confederations Cup in June.
The World Cup will be played in South Africa from June 11-July 11. The draw will be held in Cape Town on Friday.
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