Inbreeding depression is caused by increased homozygosity in the genome and merges two genetic mechanisms, a higher impact from recessive mutations and the waste of overdominance contributions. It is of major concern for the conservation of endangered populations of plants and animals, as major abnormalities are more frequent in inbred families than in outcrosses. Nevertheless, we lack appropriate analytical methods to estimate the hidden inbreeding depression load (IDL) in the genome of each individual. Here, a new mixed linear model approach has been developed to account for the inbreeding depression-related background of each individual in the pedigree. Within this context, inbred descendants contributed relevant information to predict the IDL contained in the genome of a given ancestor; moreover, known relationships spread these predictions to the remaining individuals in the pedigree, even if not contributing inbred offspring. Results obtained from the analysis of weaning weight in the MARET rabbit population demonstrated that the genetic background of inbreeding depression distributed heterogeneously across individuals and inherited generation by generation. Moreover, this approach was clearly preferred in terms of model fit and complexity when compared with classical approaches to inbreeding depression. This methodology must be viewed as a new tool for a better understanding of inbreeding in domestic and wild populations.