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Inbreeding depression is of major concern in declining populations, but relatively little is known about its genetic architecture in wild populations, such as the degree to which it is composed of large or small effect loci and their distribution throughout the genome. We combine fitness and genomic data from a wild population of red deer to investigate the genomic distribution of inbreeding effects. Inspired by the runs of homozygosity (ROH)-based inbreeding coefficient, F_ROH, we use chromosome-specific inbreeding coefficients (F_ROHChr) to explore whether the effect of inbreeding varies between chromosomes. Under the assumption that within an individual the probability of being identical-by-descent is equal across all chromosomes, we used a multi-membership model to estimate the deviation of F_ROHChrfrom the average inbreeding effect. This novel approach ensures effect sizes are not overestimated whilst maximising the power of our available dataset containing >35,000 autosomal SNPs. We find that most chromosomes confer a minor reduction in fitness-related traits, which when these effects are summed, results in the observed inbreeding depression in birth weight, survival and lifetime breeding success. However, no chromosomes had a significantly detrimental effect compared to the overall effect of inbreeding. We conclude that in this population, inbreeding depression is the result of multiple mild or moderately deleterious mutations spread across all chromosomes. As predicted by genetic theory these mutations will be inefficiently purged, explaining the persistence of inbreeding depression in this population.