The success and sustainability of control measures aimed at reducing the transmission of mosquito-borne diseases will depend on how they influence the fitness of mosquitoes in targeted populations. We investigated the effects of the micro-sporidian parasite Vavraia culicis on the survival, blood-feeding behaviour and reproductive success of female Aedes aegypti mosquitoes, the main vector of den-gue. Infection reduced survival to adulthood and increased adult female mosquito age-dependent mortality relative to uninfected individuals; this additional mortality was closely correlated with the number of parasite spores they harboured when they died. In the first gonotrophic cycle, infected females were less likely to blood-feed, took smaller meals when they did so, and developed fewer eggs than uninfected females. Even though the conditions of this laboratory study favoured minimal developmental times, the costs of infection were already being experienced by the time females reached an age at which they could first reproduce. These results suggest there will be selection pressure for mosquitoes to evolve resistance against this pathogen if it is used as an agent in a control program to reduce the transmission of mosquito-borne human diseases.