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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 [5]. 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 …