Across the globe, for oysters to persist they will need to rapidly respond to climate change. Whether oysters have sufficient adaptive capacity through the mechanism of transgenerational plasticity (TGP) is unknown but now the leading-edge of international marine climate change research, providing hope that oysters and other marine organisms may persist. Despite its promise, most studies have focussed on measuring the TGP response of a species in a single population and not considered variation among populations. Using the unique resource of pair-mated families of the Sydney Rock Oyster, Saccostrea glomerata, this study measured whether variation in TGP responses to ocean acidification exist among genotypes. Parents of four families of S. glomerata were exposed to ocean acidification (1000 µatm) during reproductive conditioning and the TGP response of their offspring was measured. Significant variation in TGP responses were observed among families, with positive, to neutral and even negative responses. The results of this study suggest that continued focus on the TGP response to climate change at the population level alone is fraught with uncertainty. If we are to secure future ecological and food services, then there remains an urgent need to explore the adaptive capacity of oysters challenged by climate change.