In a scientifically-transformative project, South Africa implemented a decade-long field experiment to understand how fisheries may be affecting its most iconic seabird, the African penguin Spheniscus demersus. This unique effort prohibits the take of anchovy and sardine within relatively small areas around four African penguin breeding colonies, two in the Benguela upwelling ecosystem and two in the adjacent Agulhas region. For the Benguela, fisheries closures within the birds’ primary foraging range increased their breeding productivity and perhaps reduced parental foraging efforts, indicating that the fisheries are competing with the birds for food. Results were less clear for foraging behaviour in the Agulhas, but no data on breeding success were collected there. The African penguin is endangered, its population continues to decline, and fisheries closures have been demonstrated to improve demographic traits that contribute to population growth. Therefore, given the critical status of the species, fisheries closures should be maintained, at least at Dassen Island where the population has great capacity to expand and support other nearby colonies. Continuing or implementing corresponding fisheries closures in the Agulhas region is also warranted, as well as creating and testing the value of pelagic closed areas during the non-breeding season when the penguins disperse widely across these ecosystems. These management actions would increase penguin food supplies and may help to meet societal goals of halting the decline of the penguin population, as well as maintaining the economic and cultural services provided by fisheries and ecotourism.