Apex marine predators, such as toothed whales and large petrels and albatrosses, ingest mercury (Hg) primarily in the form of methylmercury (MeHg) via prey consumption, which they detoxify as tiemannite (HgSe). One of the most intriguing current questions in Hg research is how more abundant lower trophic level predators detoxify MeHg, particularly in marine environments where tissue Hg burdens can be elevated. To address this need, we used high energy-resolution X-ray absorption near edge structure spectroscopy paired with nitrogen (N) and Hg stable isotopes to identify the chemical forms of Hg, Hg source, and species-specific δ²⁰²Hg isotopic values in emperor penguin, a mesopredator feeding primarily on Antarctic silverfish. The penguin liver contains variable proportions of MeHg and two inorganic Hg species (IHg), Hg-dithiolate (Hg(SR)₂) and Hg-tetraselenolate (Hg(Sec)₄) complexes, each characterized by a specific isotopic value (δ²⁰²MeHg = 0.3 ± 0.2‰, δ²⁰²Hg(SR)₂ = −1.6 ± 0.2‰, δ²⁰²Hg(Sec)₄ = −2.0 ± 0.1‰). Using δ¹⁵N as tracer of food source, we show that Hg(SR)₂ is not dietary but a biochemical demethylation product of MeHg metabolism. Penguin females transfer Hg to the egg as MeHg in the egg albumen, 89% MeHg and 11% IHg in the membrane, and 32% MeHg and 68% Hg(Sec)₄ in the yolk, on average (n = 15). Despite IHg species in eggs, MeHg is the main species quantitatively transferred by the mother to the chick because of the disproportionate mass of the MeHg-rich albumen compared to the yolk (n = 18). Further research is needed to elucidate the MeHg to Hg(SR)₂ demethylation pathway firmly documented here for the first time in multicellular organisms, and to understand why the thiolate ligands are not exchanged for Se ligands to form Hg(Sec)₄, as the liver does not suffer from Se deficiency.