Aim Colonization and extinction are important drivers of island biogeography, but they are difficult to study. We used a long-term dataset to determine the mechanisms that contribute to colonization and persistence for vector-borne blood parasites in an island population of birds that regularly receives infected vagrant conspecifics and wind-assisted potential vectors from the mainland. Location Heron Island (Australia) and the Australian mainland. Methods We determined the prevalence, temporal stability and host-specificity of Haemoproteus and Plasmodium parasites in resident and mainland-vagrant silvereyes (Zosterops lateralis) on Heron Island over seven years (1999-2003 and 2012-2013). We carried out simulations using mainland infection data and vagrant arrival scenarios to test whether transmission from vagrants influences infection patterns in island residents. We tested whether variation in island parasite prevalence was predicted by abiotic factors associated with vector breeding and dispersal. Results Parasite prevalence and composition on the island varied considerably across years. Host-specialist Haemoproteus species exhibited lower prevalence than expected and frequent absence despite a high probability of arriving via vagrants. In contrast, host-generalist Plasmodium species exhibited a low probability of arriving via vagrants but were temporally persistent in island silvereyes. Increases in prevalence and diversity of Plasmodium species were associated with episodes of offshore winds. Main conclusions This study shows that parasites that are abundant in source populations do not necessarily exhibit increased colonization success via vagrant host movement. Vagrant silvereyes are not likely to shape infection patterns in island-resident silvereyes. Instead, indirect evidence of associations between weather patterns and parasite dynamics suggests that the insular parasite community may be limited by vector establishment. Our results support the hypothesis that host-specificity is important in determining a parasite's ability to persist on islands, with host-specialists at greater risk of failing to establish after their initial arrival.