Dominance over rivals, sexual attractiveness and highly efficient ejaculates are three important contributors of male fertilization success but theories about how primary and secondary sexual characters may co-evolve largely remain to be tested. We investigated how variation in a sexual signal (forehead patch size) and in sperm morphology jointly affected siring success of 70 males in a natural population of collared flycatchers. We show that the optimal sperm length to attain high relative fertilization success depended on the size of a male’s secondary sexual character. Males with small forehead patches sired more offspring in their nest when they produced long sperm and vice-versa. These results are not compatible with theories based on simple relationships between display traits and sperm “quality” but imply that the optimal fertilization strategy (and hence optimal sperm traits) differs between males even in a predominantly socially monogamous population with moderate extra-pair paternity rates. Thus, a better knowledge of the complex chain of behavioural interactions between the sexes and their gametes is needed for a complete understanding of how sexual selection operates in nature.