Epigenetic processes have been proposed as a mechanistic basis for transgenerational plasticity (TGP). In the sea urchin Strongylocentrotus purpuratus, maternal environments can induce 3–6x greater differential CpG methylation in offspring larvae relative to effects of larval developmental environments, suggesting a role for DNA methylation in TGP. However, negligible overlap has been observed between differentially methylated and differentially expressed genes (Strader et al. 2019, 2020). This prompts the question: What gene regulatory roles does DNA methylation possess during TGP, if any? We quantified DNA methylation and gene expression in S. purpuratus larvae exposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) or embryogenesis (developmental conditioning). Using a Bayesian approach, we modeled differential gene expression (DGE), alternative splicing, and transcriptional homeostasis as functions of variation in DNA methylation across distinct genomic features and chromatin accessibility states. In response to maternal conditioning, a positive effect of differential intron methylation on DGE exhibited the highest effect strength and probability relative to other regulatory modes. This effect was significantly stronger for genes with accessible transcription start sites and low transcript abundance. Differential exon methylation induced by maternal conditioning showed a significant but weak relationship with spurious intragenic transcription, revealing a possible role for DNA methylation in preserving transcriptional homeostasis. Our results support functional roles for DNA methylation during TGP and context-dependence in these effects related to genic architecture and chromatin state.