Recent estimates of growth and mortality rates in extant Chesapeake Bay, USA oyster ( Crassostrea virginica) populations are used to quantify changes in both population abundance (dN/dT) and shell accretion (dS/dT) associated with modern population demographics. The demographics of oyster populations that would be required to maintain reef accretion rates commensurate with sea level rise over geological time frames are examined using estimates of oyster longevity in pre-colonial (pre -1600) times combined with parallel estimates of pre-disease endemic mortality. The analysis demonstrates that modern populations, with their disease related, age-truncated demographics, are generally not capable of maintaining and building biogenic reefs through accretion. Estimates of filtration rates associated with Chesapeake Bay oyster populations prior to 1600 considerably underestimate actual benthic-pelagic coupling during that period. Pristine oyster populations would have supported water column turnover rates on the order of minutes to hours. Thus, the spatial footprint of oyster reefs was limited by available productivity in the estuary. Accretion rate calculations for pristine (pre-1600) oyster reefs describe the intimate relationship between benthic-pelagic coupling and the presence or absence of oyster reefs and the associated communities.