The regulation of transposable elements (TEs) requires overlapping epigenetic modifications that must be reinforced every cell division and generation. In plants, this is achieved by multiple pathways including small RNAs, DNA methylation, and repressive histone marks that act together to control TE expression and activity throughout the entire life cycle. However, transient TE activation is observed during reproductive transitions as a result of epigenome reprogramming, thus providing windows of opportunity for TE proliferation and epigenetic novelty. Ultimately, these events may originate complex TE-driven transcriptional networks or cell-to-cell communication strategies via mobile small RNAs. In this review, we discuss recent findings and current understanding of TE regulation during sexual plant reproduction, and its implications for fertility, early seed development, and epigenetic inheritance.