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Adaptation of multicellular organisms to new environments can leave distinct signatures in their genomic architecture. Although previous efforts have unveiled the dynamics of (epi)genome evolution, our understanding remains incomplete regarding how phenotypic innovation is achieved by relaxing or constraining the identity of a genome over generations while adjusting to dynamic environments. Using plants, we first compile a list of candidate epigenetic regulators which we refer to as 'epigenetic toolkit' proteins. We propose a new framework for examining the epigenetic toolkit as an evolvable trait during plant adaptation. This could predict how feedback mechanisms between (a)biotic environmental factors and innate regulation of genome architecture can destabilize the homeostatic state of a plant and thereby inherently reshape the (epi)genetic landscapes for both short- and long-term habitat adaptation.