Eggshells are a potential tool for non-lethally sampling contaminant concentrations in bird eggs, yet few studies have examined their utility to represent mercury exposure. We assessed mercury concentrations in eggshell components for 23 bird species and determined whether they correlated with total mercury (THg) in egg contents. We designed a multi-experiment analysis to examine how THg is partitioned into eggshell components, specifically hardened eggshells, material adhered to the eggshell, and inner eggshell membranes. THg concentrations in eggshells were much lower than in egg contents, and almost all of the THg within the eggshell was contained within material adhered to eggshells and inner eggshell membranes, and specifically not within calcium-rich hardened eggshells. Despite having very little mercury, THg concentrations in hardened eggshells had the strongest correlation with egg contents among all eggshell components. However, species with the same THg concentrations in eggshells had different THg concentrations in egg contents, indicating that there is no global predictive equation among species for the relationship between eggshell and egg content THg concentrations. Further, for all species, THg concentrations in eggshells decreased with relative embryo age. Although the majority of mercury in eggshells was contained within other eggshell components and not within hardened eggshells, THg in hardened eggshells can be used to estimate THg concentrations in egg contents, if embryo age and species are addressed.