Positive correlations between heterozygosity and fitness traits are frequently observed, and it has been hypothesized, but rarely tested experimentally, that parasites play a key role in mediating the heterozygosity–fitness association. We evaluated this hypothesis in a wild great tit (Parus major) population by testing the prediction that the heterozygosity–fitness association would appear in broods experimentally infested with a common ectoparasite, but not in parasite-free broods. We simultaneously assessed the effects of parental and offspring heterozygosity on nestling growth and found that body mass of nestlings close to independence, which is a strong predictor of post-fledging survival, increased significantly with nestling levels of heterozygosity in experimentally infested nests, but not in parasite-free nests. Heterozygosity level of the fathers also showed a significant positive correlation with offspring body mass under an experimental parasite load, whereas there was no correlation with the mothers’ level of heterozygosity. Thus, our results indicate a key role for parasites as mediators of the heterozygosity–fitness correlations.