The methylation of DNA is an environmentally inducible epigenetic mechanism reflecting the short‐term ecological and environmental background of populations. Marine invertebrate populations, which spread along a latitudinal cline, are particularly suitable for profiling DNA methylation, due to the heterogenous environmental conditions experienced. We used the MSAP (Methylation Sensitive Amplified Polymorphism) technique to investigate the natural variation in DNA methylation of different female’s tissues (muscle, gonads, and gills) and early-stage eggs from five populations of the kelp crab Taliepus dentatus, distributed along a latitudinal cline in the coast of Chile. We assessed whether, (1) the distribution of DNA methylation profiles can be associated with the temporal variability of long term (18 years) climatologies (sea surface temperature, turbidity and productivity) and (2) the epigenetic diversity of eggs is related to the population-level phenotypic variability of several maternal investment traits (egg volume, egg weight, egg lipids and fecundity). The DNA methylation of eggs correlated positively and negatively with the long term variability in productivity and sea surface temperature, respectively. Furthermore, the diversity of DNA methylation of eggs correlated positively with the population-level phenotypic variability of several maternal investment traits, suggesting a key role of epigenetic mechanisms in generating phenotypic variability at population level for this species. We provide evidence of a strong link between the temporal variability of long term climatologies with the epigenetic profiles of key early ontogenetic traits associated with the maternal investment of kelp crabs. These modulating mechanisms can hence contribute early to phenotypic variability at population levels in response to local and past environmental fluctuation.