Horizontally transmitted parasites are broadly predicted to be more virulent, or costly to host fitness, than those with vertical transmission. This is mainly because vertical transmission, from host parent to offspring, explicitly links the reproductive interests of both parties. Underlying this prediction is a general assumption that parasite transmission success is positively correlated with its virulence. We report results where infection of larval yellow fever mosquitoes Aedes aegypti with the microsporidian Edhazardia aedis was experimentally manipulated. The parasite's complex life cycle allowed comparisons between estimates of horizontal and vertical transmission on host fitness. Our measure of virulence was the fluctuating asymmetry (FA) of adult female wings. Hosts harbouring spores showed higher FAs than controls. Horizontally transmitting spores were associated with higher FAs than vertically transmitting spores. Furthermore, within hosts FA correlated positively with the number of horizontally transmitting spores, while no relation was seen with the number of vertically transmitting spores. A developmental mechanism uncoupling the relationship between vertical transmission and virulence is proposed.