Carbonate mineralogies have oscillated between aragonite and calcite seas through geological time, proposed to be due mainly to secular variation in the magnesium/calcium ratio driven by changing rates of ocean crust production. A quantitative compilation of inorganic and biominerals from the onset of biomineralization (late Ediacaran–Middle Ordovician) reveals a correspondence between seawater chemistry and the first adopted mineralogy of skeletal clades. Ediacaran–Tommotian skeletons and inorganic precipitates were composed exclusively of aragonite or high-Mg calcite, but these were replaced by low-Mg calcite mineralogies during the early Atdabanian, implying the onset of a calcite sea. This transition is empirically constrained by fluid inclusion data. Late Atbadanian–Botoman inorganic precipitates returned to aragonite, with high-Mg calcite echinoderms and solitary tabulaconids and massive aragonitic tabulaconids originating during this interval. Middle Cambrian–Ordovician inorganic precipitates were low-Mg calcite, and the Ordovician radiation in skeletal expression was due mostly to groups with low-Mg calcite mineralogies. These short-lived transitions can be most parsimoniously explained by minor oscillations of mMg:Ca around ~2 during this period, possibly combined with the progressive onset of greenhouse conditions during the mid-Late Cambrian.