Transposable elements are vectors of recurrent transgenerational epigenetic inheritance.

DNA methylation loss at transposable elements (TEs) can affect neighboring genes and be epigenetically inherited in plants, yet the determinants and importance of this additional system of inheritance are unknown. In this work, we demonstrate in Arabidopsis thaliana that transgenerational stability of experimentally induced hypomethylation at TE loci is constrained by small RNAs derived from related copies. Using data from more than 700 strains collected worldwide, we uncover similar and recurrent hypomethylation at hundreds of these TE loci, often near genes. Most natural epivariants that we tested can be inherited without DNA sequence changes and are therefore bona fide epialleles, although genetic factors modulate their recurrence or persistence. Epiallelic variants often cause gene expression changes and may be targets of selection, revealing their contribution to heritable phenotypic variation in nature.