Bacterial symbionts infect the reproductive tissues of arthropods, including many economically important species that have a haplodiploid reproductive mode. By inducing various reproductive phenotypes, these symbionts often act as inheritable selfish elements for haplodiploid hosts. Previous work indicates that hosts can counteract symbiont-mediated reproductive phenotypes. Yet, despite the fundamental and applied importance of reproductive symbiosis, the molecular-genetic mechanisms underlying these host-symbiont interactions remain poorly understood. We will unravel the mechanistic underpinnings that shape the expression of reproductive phenotypes from the perspective of symbiont and host. We will take advantage of haplodiploid model systems that recently became amenable to such a genetics research endeavour. We will advance biological theory, identify novel pest control opportunities, and bridge pertinent gaps in our mechanistic understanding of reproductive symbiosis.