Unravelling plant responses to rising atmospheric CO₂ concentration ([CO₂]) has largely focussed on plastic functional attributes to single generation [CO₂] exposure. Quantifying the consequences of long‐term, decadal multigenerational exposure to elevated [CO₂] and the genetic changes that may underpin evolutionary mechanisms with [CO₂] as a driver remain largely unexplored. Here, we investigated both plastic and evolutionary plant responses to elevated [CO₂] by applying multi‐omic technologies using populations of Plantago lanceolata L., grown in naturally high [CO₂] for many generations in a CO₂ spring. Seed from populations at the CO₂ spring and an adjacent control site (ambient [CO₂]) were grown in a common environment for one generation, and then offspring were grown in ambient or elevated [CO₂] growth chambers. Low overall genetic differentiation between the CO₂ spring and control site populations was found, with evidence of weak selection in exons. We identified evolutionary divergence in the DNA methylation profiles of populations derived from the spring relative to the control population, providing the first evidence that plant methylomes may respond to elevated [CO₂] over multiple generations. In contrast, growth at elevated [CO₂] for a single generation induced limited methylome remodelling (an order of magnitude fewer differential methylation events than observed between populations), although some of this appeared to be stably transgenerationally inherited. In all, 59 regions of the genome were identified where transcripts exhibiting differential expression (associated with single generation or long‐term natural exposure to elevated [CO₂]) co‐located with sites of differential methylation or with single nucleotide polymorphisms exhibiting significant inter‐population divergence. This included genes in pathways known to respond to elevated [CO₂], such as nitrogen use efficiency and stomatal patterning. This study provides the first indication that DNA methylation may contribute to plant adaptation to future atmospheric [CO₂] and identifies several areas of the genome that are targets for future study.