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Recent research has revealed well over 1000 mtDNA lineages of avian haemosporidian parasites, but the extent to which this diversity is caused by host–parasite coevolutionary history or environmental heterogeneity is unclear. We surveyed haemosporidian and host mtDNA in a geographically structured, ecological generalist species, the house wren Troglodytes aedon, across the complex landscape of the Peruvian Andes. We detected deep genetic structure within the house wren across its range, represented by seven clades that were between 3.4–5.7% divergent. From muscle and liver tissue of 140 sampled house wrens we found 23 divergent evolutionary lineages of haemosporidian mtDNA, of which ten were novel and apparently specific to the house wren based on searches of haemosporidian databases. Combined and genus-specific haemosporidian abundance differed significantly across environments and elevation, with Leucocytozoon parasites strongly associated with montane habitats. We observed spatial stratification of haemosporidians along the west slope of the Andes where five lineages were restricted to non-overlapping elevational bands. Individual haemosporidian lineages varied widely with respect to host specificity, prevalence, and geographic distribution, with the most host-generalist lineages also being the most prevalent and widely distributed. Despite the deep divergences within the house wren, we found no evidence for host-specific co-diversification with haemosporidians. Instead, host-specific haemosporidian lineages in the genus Haemoproteus were polyphyletic with respect to the New World parasite fauna and appeared to have diversified by periodic host-switches involving distantly related avian species within the same region. These host-specific lineages appeared to have diversified contemporaneously with Andean house wrens. Taken together, these findings suggest a model of diffuse co-diversification in which host and parasite clades have diversified over the same time period and in the same geographic area, but with parasites having limited or ephemeral host specificity.