The collapse of the native oyster Crassostrea virginica fishery along the eastern United States has prompted resource managers to consider introducing a nonnative oyster for restoration of the wild fishery and/or for culture as a nonreproductive triploid. Evaluation of the profitability of a medium-sized C. ariakensis culture operation (500,000 oysters per year on ∼3 acre lease), assuming constancy of present market price despite increased supply, indicated that grow-out over winter resulted in an estimated ∼27% to 29% return on the annual investment at salinities >10 ppt because survivorship was high and Polydora spp. infestation did not occur. The greater cost of a longer grow-out phase at intermediate (10–25 ppt) salinities compensated for slightly higher mortality rates at high (>25 ppt) salinity sites, such that profitability did not vary with salinity during winter. In contrast, operations in summer always lost revenue (−28 to −37% return on investment) because of higher mortality rates at high salinities and elevated Polydora spp. infestation rates at intermediate salinities rendering the blistered oysters unsuitable for the half-shell market. Solving both the Polydora and survivorship problems would suffice to render summer operations profitable. Purchase of larger (>25 mm SH) seed from hatcheries reduced the return on investment by ∼60% in comparison with purchase and further nursery rearing of smaller (3 mm SH) seed in 2-mm mesh bags at the grow-out site. Operations utilizing larger seed were, however, still profitable (11% to 12% return on investment) during winter grow-out, and are less risky than including a nursery phase. Although Polydora infestation did not occur during the winter, sensitivity analysis determined that culture operations are extremely sensitive to Polydora spp. infestation. For instance, our analyses suggest that operations with infestation rates greater than 54% would lose revenue. Therefore, growers must avoid extending production especially at intermediate-salinity sites where grow-out is slower into the summer months when Polydora spp. settlement typically occurs. Given the economic viability of culturing C. ariakensis oysters, the potential value of the aquaculture fishery must now be considered in a broader context of the economic and ecosystem risks and benefits associated with introducing a nonnative oyster versus not introducing but instead restoring the native oyster.