Cell communication via signalling exchange plays a pivotal role in multicellular development for building functional tissues and organs. In theDrosophilatestis, a pair of somatic cyst cells (CCs) encapsulate the germline that differentiates through close-range EGFR signalling activation. The conserved Dlg/Scrib/Lgl cortical polarity complex and clathrin-mediated endocytosis attenuate EGFR signalling in CCs and loss of their function leads to EGFR overactivation and non-autonomous death of the neighbouring germ cells. Here we show that EGFR overactivation results in upregulation of JNK and p38 signalling in CCs and ROS levels in the germ cells that are destined to die. Our data uncover a bidirectional feedback between JNK signalling and ROS who regulate each other within the CC-germline microenvironment, while reducing the levels of either JNK or ROS restores germ cell survival. This study provides a framework of how polarity and cellular trafficking regulate the output of multiple signalling responses cell-intrinsically and in adjacent cells, to coordinate tissue-specific responses and maintain homeostasis.