The processes underlying parasite diversification remain largely unknown, despite the rapid accumulation of host-parasite cophylogenetic studies. Cophylogeny provides a powerful framework for studying parallel evolutionary histories of distantly related taxa over vast expanses of time, but the patterns recovered do not reveal the underlying processes. What drives diversification of directly transmitted ectoparasites? Parasite natural history traits may underly the patterns, but these hypotheses remain largely untested. Over one decade ago, a population genetics approach was proposed as a framework for studying parasite speciation. Its theoretical and analytical framework was recently updated, though with few available empirical examples, it remains largely unexplored. We show that parasite life history and ecology can be used to predict microevolutionary patterns of five co-occurring ectoparasites species from a single, endemic host species, the Galápagos Hawk (Buteo galapagoensis), in the Galápagos Islands. The ectoparasites included two ischnoceran lice, an amblyceran louse, a lousefly, and an epidermoptid skin mite that uses the lousefly as an obligate vector. We compared patterns of population genetic structure, gene flow and population divergence times among island populations for each of these ectoparasites, which exhibited wide variation in host specificity, population size, fecundity and vagility. The population genetic patterns exhibited by the parasites matched our predictions well, supporting the premise that parasite natural history drives ectoparasite microevolutionary patterns. For example, one of the host-specific ischnocerans (Degeeriella regalis) harbored the most genetic variation and population genetic structure among islands, tracked the host’s pattern of gene flow and revealed information about the host’s genealogy. This study illustrates how a population genetics approach can be used to study parasite speciation in a natural system.