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Wolbachia manipulate the reproduction of their arthropod hosts in a variety of ways. Recent work has demonstrated that these bacteria may combine phenotypes – possessing a ‘male killing’ phenotype and, where males survive, induce cytoplasmic incompatibility (CI). We here develop a mathematical model to investigate the extent to which ‘hidden’ CI may affect the evolutionary dynamics of host genes that suppress male-killing activity. We observed that for high prevalence infections, CI drives both suppressor and bacterium to higher frequency, such that the strain appears to solely exhibit CI. In contrast, for low prevalence infections, CI impedes suppressor invasion as surviving infected males are incompatible with the majority of females in the population. Our results demonstrate that ‘hidden’ phenotypes as well as observable ones can impact on the dynamics of the interaction, and knowledge of these is therefore required to predict when suppressor genes will invade, and the consequences of their invasion.