Indirect genetic effects (IGEs) exist when there is heritable variation in one species ability to alter a second species traits. For example, parasites can evolve disparate strategies to manipulate host immune response, whether by evading detection or suppressing immunity. A complication arises during coinfection, when two or more parasite genotypes may try to impose distinct IGEs on the same host trait: which parasites IGE will be dominant? Here, we apply the notion of dominance to IGEs during coinfection. Using a mathematical model we show that the dominance of IGEs can alter the evolutionary dynamics of parasites. We consider a resident parasite population receiving rare immigrants with a different immune manipulation trait. These immigrants relative fitness depends on resident prevalence (e.g., the probability immigrants are alone in a host, or coinfecting with a native), and the dominance of the immigrants IGE on host immunity. Next, we show experimentally that the cestode Schistocephalus solidus exerts an IGE on a host immune trait: parasite antigens from different populations produced different intensities of fibrosis. We then evaluated IGE dominance, finding evidence for overdominance (coinjected antigens induced an even stronger host immune response) which would be detrimental to immigrants when resident prevalence is high. This combination of experimental and modeling results shows that parasites do exhibit IGEs on host traits, and that the dominance of these IGEs during coinfection can substantially alter parasite evolution.