Background: If a parasite is able to transmit horizontally or vertically, which transmission mode will it choose? We investigated how the growth conditions and the genotype of the mosquito Aedes aegypti affect the transmission mode of the parasite Edhazardia aedis. Results: In poor conditions the parasites were more likely to be transmitted horizontally, whereas in favourable conditions they were more likely to be transmitted vertically. This plasticity appears to be adaptive. Unfavourable conditions delayed emergence, giving the parasite more time to produce its horizontally transmitted stage; in more favourable conditions mosquitoes have greater reproductive success, increasing the effectiveness of vertical transmission. In addition, the parasite's ability to transmit vertically was influenced by the genetic background of the host (i.e., its full-sib family), giving a genetic correlation between the host's life-history and which of the parasite's transmission mode it enables. In particular, genotypes with large bodies (and therefore high fecundity) were more likely to enable vertical transmission than genotypes with small bodies. This led to a trade-off among the host's families (which can be interpreted as a genetic correlation) for the parasite's transmission mode. Conclusions: Since horizontal transmission is linked to higher virulence than vertical transmission, the host's contribution to transmission mode has important consequences for the evolution of parasites with mixed-mode transmission.