Host individuals are commonly coinfected with multiple parasite species that may interact to shape within-host parasite community structure. In addition to within-host species interactions, parasite communities may also be structured by other processes like dispersal and ecological drift. The timing of dispersal (in particular, the temporal sequence in which parasite species infect a host individual) can alter within-host species interactions, setting the stage for historical contingency by priority effects, but how persistently such effects drive the trajectory of parasite community assembly is unclear, particularly under continued dispersal and ecological drift. We tested the role of species interactions under continued dispersal and ecological drift by simultaneously inoculating individual plants of tall fescue with a factorial combination of three symbionts (two foliar fungal parasites and a mutualistic endophyte), then deploying the plants in the field and tracking parasite communities as they assembled within host individuals. In the field, hosts were exposed to continued dispersal from a common pool of parasites, which should promote convergence in the structure of within-host parasite communities. Yet, analysis of parasite community trajectories found no signal of convergence. Instead, parasite community trajectories generally diverged from each other, and the magnitude of divergence depended on the initial composition of symbionts within each host, indicating historical contingency. Early in assembly, parasite communities also showed evidence of drift, revealing another source of among-host divergence in parasite community structure. Overall, these results show that both historical contingency and ecological drift contributed to divergence in parasite community assembly within hosts.