Hybridization is not a mere reproductive dead end but has been suggested to play a central role in speciation, for example, by introducing adaptive genetic variation. Our previous study uncovered a unique consequence of hybridization in Formica ants. In a population including two isolated but partially introgressed genetic groups, the females have an apparent hybrid background, whereas the males do not. This situation results in large-scale differences between male and female genomes that are stable throughout generations. Here, we compare genotypes from different developmental stages to investigate how sex-specific introgression and genetic differences between sexes are maintained. We show that strong selection rather than sex-dependent transmission maintains the genetic differences between sexes. All genotype combinations are produced and observed in the eggs of both sexes, but the alleles acquired through hybridization disappear from the haploid males during development from egg to adult as their frequencies drop toward zero. However, the same introgressed alleles increase in frequency and are favored when heterozygous in the females. Genotypes eliminated from males most likely represent incompatibilities arising from hybridization. Our results show an unusual situation of opposite selection, where introgression is favored in diploid females but selected against in haploid males. This finding suggests that introgressed genomic regions harbor both fitness-enhancing and -reducing elements. Our work highlights the complex consequences of hybridization and provides a rare opportunity to observe natural selection in real time in nature.