Native Hawaiian forest birds are experiencing an unprecedented extinction crisis. In particular, the iconic Hawaiian honeycreeper radiation has declined to just 17 out of ∼60 species remaining, most threatened with extinction due to avian malaria. Here, we investigate the genomic signatures of these declines in three honeycreeper species: the critically endangered ʻakikiki (Oreomystis bairdi) and ʻakekeʻe (Loxops caeruleirostris) and the extinct poʻouli (Melamprosops phaeosoma). Surprisingly, we find that Hawaiian honeycreepers, even the last known po‘ouli individual, maintain high heterozygosity compared with other island birds, reflecting historically large population sizes. This high heterozygosity may contribute to an elevated impact of inbreeding depression, as evidenced by reduced survival and reproductive success among highly inbred ‘akikiki. Demographic analysis revealed that recent precipitous declines in ‘akikiki and ‘akekeʻe coincide with the spread of avian malaria in the late 20^th century, consistent with malaria being the primary driver of population collapse. Using predictive population viability modeling, we explore potential recovery scenarios for ʻakekeʻe, which has recently declined below 100 individuals in the wild. Our models predict that, under current conditions, ‘akekeʻe is likely to go extinct in the near future. However, if mosquito control campaigns are effective at reducing malaria, recovery can still occur. These findings emphasize the urgency of ongoing mosquito control efforts, demonstrating hope for a species nearing the brink of extinction. More broadly, our study provides a detailed examination of genomic diversity, inbreeding depression, and extinction risk in a collapsing adaptive radiation, with implications for conservation of other endangered island species.