Climate change is driving increasingly frequent and severe rainfall, causing rapid salinity reductions in coastal and estuarine environments and potential harm to the physiology and survival of marine organisms. Transgenerational plasticity (TGP) is a rapid acclimation mechanism that may protect marine organisms against novel conditions and contend with the rate of climate change. Yet, few studies have considered TGP as a mechanism to buffer marine organisms against climate change-induced salinity reductions. This study exposed adults of ecologically and economically important oyster, Saccostrea glomerata, to control (33) and reduced (25, 20) salinity, in a fully orthogonal design, for seven weeks during reproductive conditioning. We measured the impact of this exposure on adult oysters, and the TGP response of their embryo and larval offspring. Reduced salinity had no effect on gametogenesis, growth, standard metabolic rate, or survival of adult S. glomerata. TGP effects in offspring were adaptive for some traits and maladaptive for others, dependant on whether the parent-offspring salinity environment was matched or mismatched. These results suggest that TGP responses of S. glomerata embryos and larvae to climate change-induced salinity reductions are complex and may both buffer and accelerate the negative impacts of reduced salinity on S. glomerata populations this century.