DNA methylation undergoes distinct reprogramming during plant reproductive development. Our research demonstrates that the Arabidopsis thaliana male germline establishes de novo methylation, which regulates gene expression and ensures proper meiosis. Notably, this methylation is guided by small RNAs transcribed from transposons with imperfect sequence homology. These small RNAs are not produced by meiocytes but by their nurse cells in the anther, known as the tapetum. By directing methylation and silencing transposons, the tapetum ensures both meiotic progression and the integrity of the paternal genome inherited through sexual reproduction. These findings uncover a key epigenetic mechanism that drives methylation reprogramming and promotes successful sporogenesis.