Microsporidian parasites are being considered as alternatives to conventional insecticides for malaria control. They should reduce malaria transmission by shortening the lifespan of female mosquitoes and thus killing them before they transmit malaria. As the parasite replicates throughout the mosquito’s life, it should have little detrimental effects on young mosquitoes, thus putting less selection pressure on the hosts to evolve resistance. Here, we examined these expectations for the microsporidian Vavraia culicis on Anopheles gambiae Giles sensu stricto mosquitoes under varying environmental conditions. Infection by the microsporidian delayed pupation by 10%, decreased fecundity by 23% and reduced adult lifespan by 27%, with higher infectious doses causing greater effects. The decrease of lifespan was mostly because of an increase of the mortality rate with age. Similarly, the parasite’s effect on mosquito fecundity increased with the mosquitoes’ age. Neither infection nor food availability affected juvenile survival. Thus, as V. culicis reduced the longevity of A. gambiae (s.s.), yet affected mortality and fecundity of the young mosquitoes only slightly, the microsporidian is a promising alternative to insecticides for effective malaria control that will impose little evolutionary pressure for resistance.