Intraspecific variation may shape colonization of new habitat patches through a variety of mechanisms. In particular, trait variation among colonizing individuals can produce intraspecific priority effects (IPEs), where early arrivers of a single species affect the establishment or growth of later conspecifics. While we have some evidence for the importance of IPEs, we lack a general understanding of factors affecting their presence or magnitude across a landscape. Specifically, IPEs should depend strongly on success of colonizers in the new habitat patch. This success hinges on interactions between colonizer traits and local selective pressures, but such context dependence remains unexplored experimentally. We addressed this gap by looking for the dynamical signature of IPEs in environments with and without a selective (parasite) pressure. We tested whether IPEs affected the population dynamics of a zooplankton host species (Daphnia dentifera) collected from two populations showing a tradeoff between growth rate and resistance to a fungal parasite (Metschnikowia bicuspidata). Differences in arrival order significantly altered population growth during a period of rapid resource depletion, driving large (up to 65%) differences in population abundance. Furthermore, the presence of IPEs was context dependent, as parasites reduced the impact of early arrivers on later arrivers. Such context-dependent IPEs, mediated by colonizer traits, colonization order, and selective pressures, may play an unanticipated role in the ecological and evolutionary dynamics of natural metapopulations. This mechanism highlights the overall importance of intraspecific variation for understanding ecological patterns.