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The spread of parasites and the emergence of disease are currently threatening global biodiversity and human welfare. To address this threat, we need to better understand those factors that determine parasite persistence and prevalence. It is known that dispersal is central to the spatial dynamics of host–parasite systems. Yet past studies have typically assumed that dispersal is a species-level constant, despite a growing body of empirical evidence that dispersal varies with ecological context, including the risk of infection and aspects of host state such as infection status (parasite-dependent dispersal; PDD). Here, we develop a metapopulation model to understand how different forms of PDD shape the prevalence of a directly transmitted parasite. We show that increasing host dispersal rate can increase, decrease or cause a non-monotonic change in regional parasite prevalence, depending on the type of PDD and characteristics of the host–parasite system (transmission rate, virulence, and dispersal mortality). This result contrasts with previous studies with parasite-independent dispersal which concluded that prevalence increases with host dispersal rate. We argue that accounting for host dispersal responses to parasites is necessary for a complete understanding of host–parasite dynamics and for predicting how parasite prevalence will respond to changes such as human alteration of landscape connectivity. This article is part of the theme issue ‘Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics’.