Altitudinal movement by tropical birds to track seasonally variable resources can move them from protected areas to areas of increased vulnerability. In Hawaiʻi, historical reports suggest that many Hawaiian honeycreepers such as the ‘I‘iwi (Drepanis coccinea) once undertook seasonal migrations, but the existence of such movements today is unclear. Because Hawaiian honeycreepers are highly susceptible to avian malaria, currently minimal in high-elevation forests, understanding the degree to which honeycreepers visit lower elevation forests may be critical to predict the current impact of malaria on population dynamics and how susceptible bird populations may respond to climate change and mitigation scenarios. Using radio telemetry data, we demonstrate for the first time that a large fraction of breeding adult and juvenile ‘I‘iwi originating from an upper-elevation (1,920 m) population at Hakalau Forest National Wildlife Refuge exhibit post-breeding movements well below the upper elevational limit for mosquitoes. Bloom data suggest seasonal variation in floral resources is the primary driver of seasonal movement for ‘I‘iwi. To understand the demographic implications of such movement, we developed a spatial individual-based model calibrated using previously published and original data. ʻI‘iwi dynamics were simulated backward in time, to estimate population levels in the absence of avian malaria, and forward in time, to assess the impact of climate warming as well as two potential mitigation actions. Even in disease-free ‘refuge’ populations, we found that breeding densities failed to reach the estimated carrying capacity, suggesting the existence of a seasonal “migration load” as a result of travel to disease-prevalent areas. We predict that ‘I‘iwi may be on the verge of extinction in 2100, with the total number of pairs reaching only ~ 0.2–12.3% of the estimated pre-malaria density, based on an optimistic climate change scenario. The probability of extinction of ‘I‘iwi populations, as measured by population estimates for 2100, is strongly related to their estimated migration propensity. Long-term conservation strategies likely will require a multi-pronged response including a reduction of malaria threats, habitat restoration and continued landscape-level access to seasonally variable nectar resources.