Oysters have unique life history strategies among molluscs and a long history in the fossil record. The Ostreid form, particularly species from the genus Crassostrea, facilitated the invasion into intertidal, estuarine habitats and reef formation. While there is general acknowledgement that oysters have highly variable growth, few studies have quantified variability in oyster allometry. This project aimed to (1) describe the proportional carbonate contributions from each valve and (2) examine length–weight relationships for shell and tissue across an estuarine gradient. We collected 1122 C. virginica from 48 reefs in eight tributaries and the main stem of the Virginia portion of the Chesapeake Bay. On average, the left valve was responsible for 56% of the total weight of the shell, which was relatively consistent across a size range (24.9–172 mm). Nonlinear mixed-effects models for oyster length–weight relationships suggest oysters exhibit allometric growth (b < 3) and substantial inter-reef variation, where upriver reefs in some tributaries appear to produce less shell and tissue biomass on average for a given size. We posit this variability may be due to differences in local conditions, particularly salinity, turbidity, and reef density. Allometric growth maximizes shell production and surface area for oyster settlement, both of which contribute to maintaining the underlying reef structure. Rapid growth and intraspecific plasticity in shell morphology enabled oysters to invade and establish reefs as estuaries moved in concert with changes in sea level over evolutionary time.