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Despite considerable theoretical advances in the evolutionary biology of host–parasite systems, our knowledge of host–parasite coevolution in natural systems is often limited. Among the reasons for the lag of experimental insight behind theory is that the parasite's virulence is not a simple trait that is controlled by the parasite's genes. Rather, virulence can be expressed in several traits due to the subtle interactions between the host and the parasite. Furthermore, the host might evolve tolerance to the parasite if there is sufficient genetic variance to reduce the detrimental effect of the parasite on these traits. We studied the traits underlying virulence and the genetic potential to evolve tolerance to infection in the host–parasite system Aedes aegyptiBrachiola algerae. We reared the mosquitoes in a half-sib design, exposed half of the individuals in each full-sib family to the parasite and measured several life history traits – juvenile mortality, age at pupation and adult size – of infected and uninfected individuals. Virulence was due in large part to a delay of the mosquito's age at pupation by about 10%. Although this imposes strong selection pressure on the mosquito to resist the parasite, all of the mosquitoes were infected, implying a lack of resistance. Furthermore, although additive genetic variance was present for other traits, we found no indication of additive genetic variation for the age at pupation, nor for the delay of pupation due to infection, implying no potential for the evolution of tolerance. Overall, the results suggest that in this host–parasite system, the host has little evolutionary control over the expression of the parasite's virulence.