Plasticity enhances species fitness and survival under climate change. Ocean acidification poses a potential threat to copepods, a major zooplankton group that serves as a key link between the lower and higher trophic levels in the marine environment, yet the mechanisms underlying different adaptive responses remain poorly understood. Here we show that although elevated CO₂ can exert negative effects on reproduction of Paracyclopina nana, multigenerational plasticity can enable recovery after three generations. By integrating the methylome and transcriptome with the draft genome and undertaking DNA methylation treatments, we demonstrate the vital role of epigenetic modifications in ocean acidification responses and identify regions associated with reproductive resilience. Our results demonstrate that DNA methylation might play an important role in enhancing species fitness of copepods and that failing to consider phenotypic plasticity could lead to overestimation of species’ vulnerabilities. Copyright © 2022 The Author(s).