Heterozygosity affects mate selection and can modulate interactions among family members and their fitness-related decisions. We studied whether nestling heterozygosity affected parent–offspring interactions and sib–sib competition in the Blue Tit (Cyanistes caeruleus) while controlling for the degree of relatedness among nestlings. Demanding environmental conditions might make the detection of heterozygosity-fitness correlations easier. Thus, we also investigated whether the decision rules of family members according to offspring heterozygosity were affected by brood size, as a proxy of the strength of sibling conflict. We found that chick individual heterozygosity was positively although weakly associated with individual body mass. Mean brood heterozygosity did not predict fledging success, but broods that fledged more chicks showed a higher number of less common alleles. Interestingly, fathers, but not mothers, favored heterozygous broods with many nestlings, that is, heterozygous broods with higher potential for sibling conflict. Moreover, the lower the mean brood heterozygosity the stronger the begging intensity when parents were absent, regardless of brood size. Finally, the degree of relatedness among nestlings was not associated with any behavioral parameter, supporting a more prominent role for heterozygosity in shaping intra-family interactions. Our findings suggest that offspring heterozygosity determines sex-specific rules of parental care and that genetic diversity is associated with lower sibling competition.