In plants, transposable elements (TEs) are kept inactive by transcriptional gene silencing (TGS). TGS is established and perpetuated by RNA-directed DNA methylation (RdDM) and maintenance methylation pathways, respectively. Here, we describe a novel RdDM function specific for shoot apical meristems that reinforces silencing of TEs during early vegetative growth. In meristems, RdDM counteracts drug-induced interference with TGS maintenance and consequently prevents TE activation. Simultaneous disturbance of both TGS pathways leads to transcriptionally active states of repetitive sequences that are inherited by somatic tissues and partially by the progeny. This apical meristem-specific mechanism is mediated by increased levels of TGS factors and provides a checkpoint for correct epigenetic inheritance during the transition from vegetative to reproductive phase and to the next generation.