Transgenerational plasticity (TGP) has been identified as a critical mechanism of acclimation that may buffer marine organisms against climate change, yet whether the TGP response of marine organisms is altered depending on their habitat is unknown. Many marine organisms are found in intertidal zones where they experience episodes of emersion (air exposure) daily as the tide rises and recedes. During episodes of emersion, the accumulation of metabolic carbon dioxide (CO2) leads to hypercapnia for many species. How this metabolic hypercapnia impacts the TGP response of marine organisms to climate change is unknown as all previous transgenerational studies have been done under subtidal conditions, where parents are constantly immersed. Here, we assess the capacity of the ecologically and economically important oyster, Saccostrea glomerata, to acclimate to elevated CO2 dependent on habitat, across its vertical distribution, from the subtidal to intertidal zone. Tidal habitat altered both the existing tolerance and transgenerational response of S. glomerata to elevated CO2. Overall, larvae from parents conditioned in an intertidal habitat had a greater existing tolerance to elevated CO2 than larvae from parents conditioned in a subtidal habitat, but had a lower capacity for beneficial TGP following parental exposure to elevated CO2. Our results suggest that the TGP responses of marine species will not be uniform across their distribution and highlights the need to consider the habitat of a species when assessing TGP responses to climate change stressors.