Vertebrate embryos are exposed to maternal hormones that can profoundly affect their later phenotype. Although it is known that the embryo can metabolize these maternal hormones, the metabolic outcomes, their quantitative dynamics and timing are poorly understood. Moreover, it is unknown whether embryos can adjust their metabolic activity to, for example, hormones or other maternal signals. We studied the dynamics of maternal steroids in fertilized and unfertilized rock pigeon eggs during early incubation. Embryos of this species are naturally exposed to different amounts of maternal steroids in the egg according to their laying position, which provides a natural context to study differential embryonic regulation of the maternal signals. We used mass spectrometric analyses to map changes in the androgen and estrogen pathways of conversion. We show that the active hormones are heavily metabolized only in fertilized eggs, with a corresponding increase in supposedly less potent metabolites already within one-fourth of total incubation period. Interestingly, the rate of androgen metabolism was different between embryos in different laying positions. The results also warrant a re-interpretation of the timing of hormone mediated maternal effects and the role of the supposedly biologically inactive metabolites. Furthermore, the results also provide a potential solution as to how the embryo can prevent maternal steroids in the egg from interfering with its sexual differentiation processes as we show that the embryo can metabolize most of the maternal steroids before sexual differentiation starts.