Within‐species diversity is an important driver of ecological and evolutionary processes. Recent research has found that plants can harbour significant epigenetic diversity, but its extent, stability and ecological significance in natural populations is largely unexplored.

We analysed genetic, epigenetic and phenotypic variation in a large number of natural grassland populations of Plantago lanceolata, covering a broad geographic and environmental range. Within‐population diversity and among‐population differentiation were calculated from genetic and epigenetic marker data and from measurements of phenotypic traits, both for plants in the field and for the F₁ generation grown in a common environment.

We found weak but significant epigenetic population structure. A large part of the epigenetic population differences observed in the field was maintained in a common environment. Epigenetic differences were consistently related to genetic and environmental variation, and to a lesser degree to phenotypic variation and land use, with more grazed populations harbouring greater epigenetic diversity.

Our study demonstrates that epigenetic diversity exists in natural populations of a common grassland species, and that at least part of this epigenetic diversity is stable, non‐random and related to environmental variation. Experimental and more detailed molecular studies are needed to elucidate the mechanistic basis of these observed patterns.