Maintenance of germline genomic integrity is critical for the survival of animal species. Consequently, many cellular and molecular processes have evolved to ensure genetic stability during the production of gametes. Here, we describe the discovery, characterization, and emerging molecular mechanisms of the protein Asterix/Gametocyte-specific factor 1 (GTSF1), an essential gametogenesis factor that is conserved from insects to humans. Beyond its broad importance for healthy germline development, Asterix/GTSF1 has more specific functions in the Piwi-interacting RNA (piRNA)-RNA interference pathway. There, it contributes to the repression of otherwise deleterious transposons, helping to ensure faithful transmission of genetic information to the next generation.