Failure of the Apalachicola Bay oyster population to recover since the 2012 fishery collapse, despite a decade of unprecedented restoration efforts and a fishery closure, indicates that the system has lost its former resilience, crossed a critical threshold between ecological steady states, and is experiencing hysteresis. This commentary contributes to the weight of evidence that reflects how accumulated system stressors led to reduced resilience and alterations in the ecological state of Apalachicola Bay. Discussion of resource exploitation, negative shell budget, salinity extremes, predator abundance, parasites, and disease underscore how these stressors accumulate over time to impact oyster populations and system resilience. Additionally, various interpretations of “resilience,” “exploitation,” and “restoration” have facilitated chronic resource over-exploitation and oyster habitat degradation in Apalachicola Bay. Within this context, a necessary cultural shift is described that reframes restoration and management goals to target healthy oyster habitat as the endpoint rather than using fishery metrics based on the number of harvestable oysters per acre. Failure to reframe restoration goals may be the cumulative result of resistance to accepting the presence of ecological state change, economic drivers overshadowing the weight of evidence, and outcomes not directly impacting decision makers.