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Many malaria vector mosquitoes in Africa have an extreme preference for feeding on humans. This specialization allows them to sustain much higher levels of transmission than elsewhere, but there is little understanding of the evolutionary forces that drive this behaviour. In Tanzania, we used a semi-field system to test whether the well-documented preferences of the vectors An. arabiensis and An. gambiae s.s. for cattle and humans respectively are predicted by the fitness they obtain from host-seeking on these species relative to other available hosts. Mosquito fitness was contrasted when humans were fully exposed, and when they were protected by a typical bednet. The fitness of both vectors varied between host species. The predicted relationship between host preference and fitness was confirmed in An. arabiensis, but not in An. gambiae s.s. whose fitness was similar on humans and other mammals. Use of typical, imperfect bednets generated only minor reductions in An. gambiae s.s. feeding success and fitness on humans, but was predicted to generate a significant reduction in the lifetime reproductive success of An. arabiensis on human relative to cows. This supports the hypothesis that such human-protective measures could additionally benefit malaria control by increasing selection for zoophily in vectors.