Host-parasite cospeciation, in which parasite divergence occurs in response to host divergence, is commonly proposed as a driver of parasite diversification, yet few empirical examples of strict cospeciation exist. Host-parasite co-evolutionary histories commonly reflect complex mosaics of cospeciation, dispersal, lineage extinction and other phenomena. The episodic host-switching model of parasite diversification accounts for complexity by suggesting that diversification and faunal assembly is a consequence of fluctuation between environmental disruption and environmental stability. The phylogeographic predictions of the strict cospeciation and episodic host-switching models were tested using the North American pika/parasite assemblage, with a primary focus on the American pika, Ochotona princeps (Richardson, 1828), and a suite of its endoparasitic cestodes and nematodes. This approach integrating phylogeographic and demographic methods with inferences drawn from species distribution modelling revealed that the parasite community of pikas has been shaped by climate-driven range fluctuation of hosts and bouts of geographic and host colonization by parasites associated with transitions between glacial and interglacial phases.