We examined factors affecting the virulence of Metaphycus flavus (Hymenoptera: Encyrtidae), a facultatively gregarious endoparasitoid of Coccus hesperidum (Hemiptera: Coccidae). Clutch size significantly negatively influenced encapsulation rates of the parasitoid’s eggs by the host (in some cases encapsulation rates increased two-fold in incomplete clutches of eggs). Clutches were smaller when individuals sequentially parasitized two hosts in a patch. This resulted in increased egg encapsulation rates in the second parasitized host. Our results suggest that increased encapsulation rates in second hosts are due not entirely to clutch size, but also possibly to the depletion of chemicals with immunosuppressive properties that individual wasps inject inside hosts during oviposition. This hypothesis is also supported by the fact that 4h after the first oviposition experience wasp virulence decreased, whereas 48h after oviposition experience virulence was regained. Our results suggest that parasitoid virulence is dynamic because it is directly linked with clutch size decisions. However, clutch size in synovigenic, egg-limited parasitoids such as M. flavus is influenced by several parameters such as egg load, experience, host availability and physiological state. This study has implications for understanding how constraints on the evolution of solitary to gregarious larval development have been overcome: the allocation of multiple eggs to suppress host immune defences could serve as the first step in the transition from solitary to gregarious development. We also discuss how larval immobility within a host and other life history characteristics of this species further facilitate this transition.