Our climate is changing rapidly and organisms must either move, adapt or acclimate in order to persist. Epigenetic modifications such as DNA methylation may be an important mechanism underlying fast, adaptive responses, as they can contribute to heritable changes within populations and drive rapid evolution. Crucial during gametogenesis and development (embryogenesis), epigenetic modifications can be inherited both mitotically within a generation, and/or meiotically across generations (transgenerational epigenetic inheritance). However, heritable epigenetic modifications must overcome two reprogramming phases, once in the germline and once in the early embryo. Despite being well documented in plant and mammalian systems, epigenetic reprogramming studies during fish gametogenesis and embryogenesis have focused only on a few model species. Here, we investigated DNA methylation patterns, together with the molecular characterization and mRNA expression profiles of DNA-methyltransferase enzymes (DNMT) during gametogenesis and embryogenesis of marine threespine stickleback. Additionally, the impact of multiple simulated ocean warming scenarios (ambient °C, +1.5°C and +4°C) were evaluated at both the epigenetic and phenotypic level to establish a functional link between methylomes, epigenetic reprogramming and transgenerational plasticity, and their role in adaptive potential to climate change.