Male fertility is negatively affected by inbreeding across a wide variety of taxa, but the cause of this apparently universal fragility remains mysterious. Sperm quality (sperm count, motility and morphology) has frequently been recorded as having a negative relationship with inbreeding, but cross-species comparisons are required to establish whether this universal fragility is attributable to the same genes in all species. The relationship between inbreeding and sperm quality has rarely been assessed in wild populations, has almost exclusively focused on mammals. In birds, males are the homogametic (ZZ) rather than the heterogametic (ZW) sex and, according to Haldane’s rule, should be less susceptible to inbreeding depression than females. Here, we couple sperm quality data with extensive microsatellite genotyping to test the relationship between genetic diversity, inbreeding and sperm quality in bird populations that have experienced a range of bottleneck scenarios. Here we present data from South Island robin (Petroica australis australis) and hihi (Notiomystis cincta), both of which have experienced multiple translocation-induced bottlenecks in the past few decades. Inbred individuals of these species are known to exhibit increased nest failure compared to less inbred individuals, but the cause of this failure remains unknown. Our data suggest that at least some of these failures are due to male infertility as a result of reduced genetic diversity and increased inbreeding. We are currently assembling the South Island robin genome in an effort to identify particular genes that might be responsible for this trend to aid conservation management of these and other species.