Mate choice for genetic benefits is assumed to be widespread in nature, yet very few studies have comprehensively examined relationships between female mate choice and male genetic quality in wild populations. Here, we use exhaustive sampling and single nucleotide polymorphisms (SNPs) to provide a partial test of the “good genes as heterozygosity” hypothesis and the “genetic compatibility” hypothesis in an entire population of terrestrial breeding red-backed toadlets, Pseudophryne coriacea. We found that successful males did not display higher heterozygosity, despite a positive relationship between male heterozygosity and offspring heterozygosity. Rather, in the larger of two breeding events, we found that successful males were more genetically similar to their mate than expected under random mating, indicating that females can use pre- or post-copulatory mate choice mechanisms to bias paternity towards more related males. These findings provide no support for the good genes as heterozygosity hypothesis but lend support to the genetic compatibility hypothesis. A complete test of this hypothesis will now require evaluating how parental genetic similarity impacts offspring fitness. Terrestrial toadlets show a high degree of site fidelity, high levels of genetic structuring between populations, and frequently hybridise with sister species. As such, female mate choice for related males may be an adaptive strategy to reduce outbreeding depression. Our findings provide the first population-wide evidence for non-random preferential inbreeding in a wild amphibian. We argue that such reproductive patterns may be common in amphibians because extreme genetic differentiation within meta-populations creates an inherently high risk of outbreeding depression.