Transposons, constituting approximately 50% of the human genome, can be considered genome modifiers due to their ability to transpose themselves. However, the reasons for their existence and their significant impact on phenotypes still remain unclear. Our research has brought new insights into the regulation of transposon expression and transposition by piRNAs (PIWI-interacting RNAs). piRNAs, small non-coding RNAs of 24-30 nucleotides, are exclusively expressed in animal gonads and loaded into the PIWI clade members of the Argonaute protein family. These piRNAs act as guides for the PIWI protein and its associated complexes to induce co-transcriptional regulation of their target transposons. Through our investigations, we have revealed that PIWI-piRNA-mediated regulation not only governs the expression of transposons but also exerts a profound influence on genome structure and compartmentalization, often facilitated by the formation of heterochromatin. This dynamic regulatory mechanism profoundly shapes the landscape of the genome. Moreover, our findings have uncovered a novel enhancer-mediated regulation mechanism governing Drosophila telomeric transposons. This mechanism complements piRNA-mediated regulation, especially in somatic cells. Taking these into account, we propose a hypothesis that genomic plasticity emerges from the intricate interplay and antagonism between transposons and the regulatory mechanism.