Little is known of the capacity that marine metazoans have to evolve under rapid pCO₂ changes. Consequently, we reared a marine polychaete, Ophryotrocha labronica, previously cultured for approximately 33 generations under a low/variable pH regime, under elevated and low pCO₂ for six generations. The strain used was found to be tolerant to elevated pCO₂ conditions. In generations F1 and F2 females’ fecundity was significantly lower in the low pCO₂ treatment. However, from generation F3 onwards there were no differences between pCO₂ treatments, indicating that trans‐generational effects enabled the restoration and maintenance of reproductive output. Whilst the initial fitness recovery was likely driven by trans‐generational plasticity (TGP), the results from reciprocal transplant assays, performed using F7 individuals, made it difficult to disentangle between whether TGP had persisted across multiple generations, or if evolutionary adaptation had occurred. Nonetheless, both are important mechanisms for persistence under climate change. Overall, our study highlights the importance of multi‐generational experiments in more accurately determining marine metazoans’ responses to changes in pCO₂, and strengthens the case for exploring their use in conservation, by creating specific pCO₂ tolerant strains of keystone ecosystem species.