Mutualism is often selected in vertically transmitted symbionts due to their fitness interdependence with hosts. However, the evolution of mutualism remains unclear in symbionts using both vertical and horizontal transmission. In this study, we show that Ascogregarina taiwanensis, previously known as a weak horizontally transmitted parasite of the Asian tiger mosquito (Aedes albopictus), exhibits mutualistic traits that enhance mosquito reproduction. The symbiont improves embryogenesis and extends the egg-laying period while most females are pseudo-vertically transmitting symbiont oocysts to their progeny at oviposition sites. Dual transcriptomic analyses reveal that early oogenesis in infected females involves increased nitrogen metabolism in both partners, enhanced detoxification of blood waste, and activation of egg development pathways. These changes lead to improved assimilation of blood proteins essential for egg production. Our findings provide rare empirical evidence of a symbiont displaying both parasitic and mutualistic traits, offering new insights into the evolutionary dynamics of mixed-mode transmission symbioses.