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We studied the organization and temporal stability of an assemblage of malaria parasites (genera Plasmodium and Haemoproteus ) and their passerine avian hosts in a forested study area in southern Missouri, USA, over four years. We detected parasite infections by polymerase chain reaction (PCR) of parasite DNA from host blood samples and identified parasite lineages by sequencing a part of the mitochondrial cytochrome b gene. We obtained 757 blood samples from 42 host species. Prevalence of malaria parasitism judged by PCR averaged 38.6% and varied in parallel in the three most abundant host species over the four years of the study. Parasite prevalence bore a U‐shaped relationship to host sample size. Prevalence was weakly positively associated with host body mass, but not with foraging stratum, nest height, nest type, plumage brightness, or sexual dichromatism. Over the sample as a whole, parasite prevalence did not vary between males and females or between hatch‐year and older individuals. We differentiated 34 parasite lineages. The number of host species per lineage varied from one to eight and increased with sample size. We recovered up to 14 lineages of parasite from a single host. Three relatively common lineages in the Ozarks were found nowhere else; four others were recovered from other sites in eastern North America; and six additional well‐sampled lineages were distributed in the Greater Antilles among resident island host species. Parasites that are endemic among native species of hosts on the tropical wintering grounds of Ozark birds were recovered from hatch‐year birds in the Ozarks, indicating that transmission takes place on the summer breeding grounds, and consequently, that suitable vectors are present in both the temperate and tropical portions of the parasite lineage distributions. We estimate that the number of parasite lineages within a local area will approximate the number of host species and that our perception of host breadth and parasite diversity will increase for most lineages and hosts with increased sampling. Thus, host–parasite relationships in a local area, including the role of parasites in sexual selection and the evolutionary maintenance of sex, are likely to be complex, with population and evolutionary dynamics involving many actors.