Significance We have identified, by genetic and cytological analyses, the minimal components of a chaperone complex involved in transposon (TE) silencing in Drosophila germ cells. We found that, after heat shock, the stress-inducible Hsp70 chaperone interacts with the chaperone complex and factors involved in piRNAs biogenesis in both ovaries and testes. Hsp70 induces displacement of these factors to the lysosomes. Concomitantly, we observed a significant activation of TEs at the posttranscriptional level, suggesting an involvement of Hsp70 in TE activation after stress. We propose that such a mechanism has evolutionary implications for the genome’s response to environmental stress.