Experimental assessments of species vulnerabilities to ocean acidification are rapidly increasing in number, yet the potential for short- and long-term adaptation to high CO₂ by contemporary marine organisms remains poorly understood. We used a novel experimental approach that combined bi-weekly sampling of a wild, spawning fish population (Atlantic silverside Menidia menidia) with standardized offspring CO₂ exposure experiments and parallel pH monitoring of a coastal ecosystem. We assessed whether offspring produced at different times of the spawning season (April to July) would be similarly susceptible to elevated (~1100 µatm, pH_NIST = 7.77) and high CO₂ levels (~2300 µatm, pH_NIST = 7.47). Early in the season (April), high CO₂ levels significantly (p < 0.05) reduced fish survival by 54% (2012) and 33% (2013) and reduced 1 to 10 d post-hatch growth by 17% relative to ambient conditions. However, offspring from parents collected later in the season became increasingly CO₂-tolerant until, by mid-May, offspring survival was equally high at all CO₂ levels. This interannually consistent plasticity coincided with the rapid annual pH decline in the species’ spawning habitat (mean pH: 1 April/31 May = 8.05/7.67). It suggests that parents can condition their offspring to seasonally acidifying environments, either via changes in maternal provisioning and/or epigenetic transgenerational plasticity (TGP). TGP to increasing CO₂ has been shown in the laboratory but never before in a wild population. Our novel findings of direct CO₂-related survival reductions in wild fish offspring and seasonally plastic responses imply that realistic assessments of species CO₂-sensitivities must control for parental environments that are seasonally variable in coastal habitats.