Gene expression plasticity can confer physiological plasticity in response to the environment. However, whether or not epigenetic marks play a role in contributing to the dynamics of gene expression is still unknown in most marine invertebrates. Here, we explored the extent of, and the molecular basis of, intra- and transgenerational plasticity in the purple sea urchin, Strongylocentrotus purpuratus. Our overarching goal was to examine relationships between changes in DNA methylation, transcription, and physiological traits. Adult urchins were conditioned in the lab for four months to treatments that represent end-member regimes experienced in their local kelp forest environment: conditions that are typical for upwelling (~1100µatm, 13 °C) and those typical of non-upwelling conditions (~500µatm, 17 °C). Embryos spawned from adults in each of the two treatments were reared in either the same adult treatment or the reciprocal condition. Maternal conditioning resulted in significantly differentially methylated CpG sites and gene expression in the larvae, despite minimal evidence of maternal effects for other larval traits. Genes with differential CpG methylation were always highly methylated and tended to exhibit higher levels of transcription. In contrast, conditions experienced during embryonic development resulted in pronounced differences in body size, thermal tolerance and respiration in larvae, likely driven by differences in temperature. This intragenerational plasticity in whole organism physiological traits was strongly correlated to plasticity in the transcriptome, despite low levels of intragenerational plasticity in CpG methylation. Although there are strong differences in physiological traits, DNA methylation and transcription in response to different environmental conditions, we observed little overlap on a gene-by-gene basis. Therefore, our results suggest that different forms of environmentally induced plasticity are observable across different time scales and that DNA methylation dynamics may be uncoupled from fast transcriptional responses to the environment and whole organism physiological traits. Overall, this study illuminates the extent to which environmental differences can induce both intra- and transgenerational phenotypic plasticity in a common kelp forest herbivore.