Here, we explore enrichments in paleomarine Zn as recorded by authigenic iron oxides including Precambrian iron formations, ironstones, and Phanerozoic hydrothermal exhalites. This compilation of new and literature-based iron formation analyses track dissolved Zn abundances and constrain the magnitude of the marine reservoir over geological time. Overall, the iron formation record is characterized by a fairly static range in Zn/Fe ratios throughout the Precambrian, consistent with the shale record (Scott et al., 2013, Nature Geoscience, 6, 125–128). When hypothetical partitioning scenarios are applied to this record, paleomarine Zn concentrations within about an order of magnitude of modern are indicated. We couple this examination with new chemical speciation models to interpret the iron formation record. We present two scenarios: first, under all but the most sulfidic conditions and with Zn-binding organic ligand concentrations similar to modern oceans, the amount of bioavailable Zn remained relatively unchanged through time. Late proliferation of Zn in eukaryotic metallomes has previously been linked to marine Zn biolimitation, but under this scenario the expansion in eukaryotic Zn metallomes may be better linked to biologically intrinsic evolutionary factors. In this case, zinc‘s geochemical and biological evolution may be decoupled and viewed as a function of increasing need for genome regulation and diversification of Zn-binding transcription factors. In the second scenario, we consider Archean organic ligand complexation in such excess that it may render Zn bioavailability low. However, this is dependent on Zn–organic ligand complexes not being bioavailable, which remains unclear. In this case, although bioavailability may be low, sphalerite precipitation is prevented, thereby maintaining a constant Zn inventory throughout both ferruginous and euxinic conditions. These results provide new perspectives and constraints on potential couplings between the trajectory of biological and marine geochemical coevolution.