Although connectivity can promote host species persistence in a metapopulation, dispersal may also enable disease transmission, an effect further complicated by the impact that parasite distribution may have on host-parasite population dynamics. We investigated the effects of connectivity and initial parasite distribution (clustered or dispersed) on microparasite-host dynamics in experimental metapopulations, using guppies and Gyrodactylus turnbulli. We created metapopulations of guppies divided into four subpopulations and introduced either a low level of parasites to all subpopulations (dispersed) or a high level of parasites to one subpopulation (clustered). Controlled migration among subpopulations occurred every 10 days. In additional trials, we introduced low or high levels of parasites to isolated populations. Parasites persisted longer in metapopulations than in isolated populations. Mortality was lowest in isolated populations with low level introductions. The interaction of connectivity and initial parasite distribution influenced parasite abundance. With low level introductions, connectivity helped the parasite persist longer but had little effect on the hosts. With high levels, connectivity also benefited the hosts, lowering parasite burdens. These findings have implications for disease management and species conservation.