Understanding host-parasite interactions is of the utmost importance for disease prediction, prevention and management. Hence, this study assessed the transcriptional response of the primary malaria vector Anopheles gambiae, to infection with several lines of the candidate vector-control parasite, the microsporidian Vavraia culicis. These parasite lines were selected for early or late transmission within this host. Previous studies extensively described them phenotypically, differing in their virulence, infection dynamics and host exploitation. Using RNA sequencing, gene expression profiles were analyzed in An. gambiae mosquitoes infected with early-transmission-selected, late-transmission-selected, and unselected (Stock ) V. culicis lines, as well as in uninfected controls. The results revealed distinct transcriptional changes associated with each parasite line. Early-selected parasites induced a broader immune response than late-selected ones. Differential expression of immune-related genes, including Toll-interacting protein and Protein ERGIC-53, was identified. Additionally, significant changes were observed in pathways related to Golgi membrane function and oxidative stress response, particularly in response to early-selected parasites. These findings highlight the evolutionary pressures shaping host-parasite coevolution and provide insight into how parasite transmission traits can influence the mosquito's immune response and regulation. This work provides a foundation for future studies on mosquito-microsporidia dynamics and potential applications for vector control strategies, particularly in the context of Plasmodium control.