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Researchers have long debated which estimator of relatedness best captures the degree of relationship between two individuals. In the genomics era, this debate continues, with relatedness estimates being sensitive to the methods used to generate markers, marker quality, and levels of diversity in sampled individuals. Here, we compare six commonly used genome‐based relatedness estimators (kinship genetic distance [KGD], Wang maximum likelihood [TrioML], Queller and Goodnight [R_xy], Kinship INference for Genome‐wide association studies [KING‐robust), and pairwise relatedness [R_AB], allele‐sharing coancestry [AS]) across five species bred in captivity–including three birds and two mammals–with varying degrees of reliable pedigree data, using reduced‐representation and whole genome resequencing data. Genome‐based relatedness estimates varied widely across estimators, sequencing methods, and species, yet the most consistent results for known first order relationships were found usingR_xy,R_AB, and AS. However, AS was found to be less consistently correlated with known pedigree relatedness than eitherR_xyorR_AB. Our combined results indicate there is not a single genome‐based estimator that is ideal across different species and data types. To determine the most appropriate genome‐based relatedness estimator for each new data set, we recommend assessing the relative: (1) correlation of candidate estimators with known relationships in the pedigree and (2) precision of candidate estimators with known first‐order relationships. These recommendations are broadly applicable to conservation breeding programmes, particularly where genome‐based estimates of relatedness can complement and complete poorly pedigreed populations. Given a growing interest in the application of wild pedigrees, our results are also applicable to in situ wildlife management.