Variation in the presence or absence of transposable element (TE) insertions is a significant source of inter-individual genetic variation. Here, we identified 23,095 TE presence/absence variants between 216 wild Arabidopsis accessions. Most variants are rare, however over two thirds of the common alleles identified were not in linkage disequilibrium with nearby SNPs, implicating TE variants as a source of missing heritability. Some TE variants were associated with altered expression of nearby genes, with potential functional consequences including decreased pathogen resistance. The majority of inter-accession DNA methylation differences were associated with nearby TE variants, indicating an important role in facilitating epigenomic variation. Examination of TE regulation following crosses between parents with differential TE content revealed that absence of individual TEs from the paternal genome is associated with DNA demethylation within maternal copies of these TEs in the embryo, suggesting parental TE variation may enable activation of previously silent TEs.