Reduced fitness as a result of inbreeding is a major threat facing many species of conservation concern [1-4]. However, few case studies for assessing the magnitude of inbreeding depression in the wild means that its relative importance as a risk factor for population persistence remains under-appreciated . The increasing availability and affordability of genomic technologies provide new opportunities to address knowledge gaps around the magnitude and manifestation of inbreeding depression in wild populations [6-12]. Here, we combine over three decades of individual lifetime reproductive data and genomic data to estimate the relative lifetime and short-term fitness costs of both being inbred and engaging in inbreeding in the last wild population (<250 individuals remaining) of an iconic and critically endangered bird: the helmeted honeyeater Lichenostomus melanops cassidix. The magnitude of inbreeding depression was substantial: the mean predicted lifetime reproductive success of the most inbred (homozygosity = 0.82) individuals was on average 87%-90% lower than that of the least inbred (homozygosity = 0.75). For individual reproductive events and lifetime measures, we provide rare empirical evidence that pairing with a genetically dissimilar individual can reduce fitness costs associated with being an inbred individual. By comparing lifetime and short-term fitness measures, we demonstrate how short-term measures of reproductive success that are associated with only weak signatures of inbreeding depression can still underlie stronger lifetime effects. Our study represents a valuable case study, highlighting the critical importance of inbreeding depression as a factor influencing the immediate viability of populations in threatened species management.