Fluctuating environments threaten fertility and viability. To better match the immediate, local environment, many organisms adopt alternative phenotypic states, a phenomenon called “phenotypic plasticity.” Natural populations that predictably encounter fluctuating environments tend to be more plastic than conspecific populations that encounter a constant environment, suggesting that phenotypic plasticity can be adaptive. Despite pervasive evidence of such “adaptive phenotypic plasticity,” gene regulatory mechanisms underlying plasticity remain poorly understood. Here we test the hypothesis that environment-dependent phenotypic plasticity is mediated by epigenetic factors and that these epigenetic factors vary across naturally occurring genotypes. To test this hypothesis, we exploit the adaptive reproductive arrest of Drosophila melanogaster females, called diapause. Using an inbred line from a natural population with high diapause plasticity, we demonstrate that diapause is determined epigenetically: only a subset of genetically identical individuals enter diapause and this diapause plasticity is epigenetically transmitted for at least three generations. Upon screening a suite of epigenetic marks, we discovered that the active histone marks H3K4me3 and H3K36me1 are depleted in diapausing ovaries. Using ovary-specific knockdown of histone mark writers and erasers, we demonstrate that H3K4me3 and H3K36me1 depletion promotes diapause. Given that diapause is highly polygenic – distinct suites of alleles mediate diapause plasticity across distinct genotypes – we investigated the potential for genetic variation in diapause-determining epigenetic marks. Specifically, we asked if these histone marks were similarly depleted in diapause of a genotypically distinct line. We found evidence of divergence in both the gene expression program and histone mark abundance. This dissertation reveals chromatin determinants of phenotypic plasticity and suggests that these determinants are genotype-dependent, offering new insight into how organisms may exploit and evolve epigenetic mechanisms to persist in fluctuating environments.