Reproductive phenotypes are shaped by genetic, physiological and environmental variation that an organism experiences during ontogeny. Steroid hormones play an integrative role in this process through both genomic and non-genomic pathways. Differences in steroid hormone metabolism may be rooted in genomic variation. Here we evaluate the influence of supergene variants underlying alternative reproductive tactics on sex steroid metabolism during ontogeny in ruffs (Calidris pugnax). Adult ruff males exhibit three male mating morphs called Independents, Faeders and Satellites, that differ prominently in circulating androgen (testosterone and androstenedione) concentrations. Across morphs and sexes chicks showed similar mean androgen concentrations during ontogenetic development. However, variances in circulating androgens showed the same pattern as corresponding variances previously observed in adults. HSD17B2 had been previously identified as a key gene for mediating differences in androgen levels between morphs as it encodes the enzyme that converts testosterone to androstenedione and is located within the supergene. Observed HSD17B2 expression in embryonic brain tissue was consistent with predictions based on genetic and endocrine differences. Taken together, the observed differences in circulating androgen concentrations and gene expression point to testosterone synthesis as a key mechanism that shapes developmental trajectories and differences in brain organization among morphs.