Significant progress in our understanding of disease transmission in the wild can be made by examining variation in host-parasite-vector interactions after founder events of the host. This study is the first to document patterns in avian malaria, Plasmodium spp., infecting an endemic New Zealand passerine, Anthornis melanura, at multiple-host subpopulations simultaneously. We assess the Beaudoin hypothesis of bimodal seasonality and use AIC model selection to determine host factors associated with disease prevalence. We had the rare opportunity to test the enemy release hypothesis (ERH) after a recent colonisation event of the bellbird host. Four Plasmodium species were found to infect bellbirds. Temporal patterns of three exotic parasite lineages, including GRW06 Plasmodium (Huffia) elongatum, SYAT05 Plasmodium (Novyella) vaughani and a Plasmodium (Haemamoeba) relictum, were sporadic with low prevalence year round. The fourth species was an endemic parasite, an unresolved Plasmodium (Novyella) sp. here called ANME01, which exhibited a strong winter peak at the source subpopulations possibly indicating greater immune stressors at the densely populated source site. At the colonies, we observed bimodal seasonality in the prevalence of ANME01 with autumn and spring peaks. These infection peaks were male-biased, and the amplitude of sex bias was more pronounced at the newer colony perhaps due to increased seasonal competition resulting from territory instability. We observed a decrease in parasite species diversity and increase in body condition from source to founder sites, but statistical differences in the direct relationship between body condition and malaria prevalence between source and colony were weak and significant only during winter. Though our data did not strongly support the ERH, we highlight the benefits of 'conspecific release' associated with decreased population density and food competition. Our findings contribute to the identification of ecological and environmental drivers of variability in malaria transmission, which is valuable for predicting the consequences of both natural range expansions, as well as host re-introductions resulting from intensive conservation practices.