Self-renewing organs require balanced rates of cell production and loss to maintain a constant number of cells. Cellular imbalance leads to organ hyperplasia or degeneration, but how cellular balance is enforced during normal renewal remains poorly understood. Examining intestinal renewal in Drosophila, we find that feedback inhibition from mature enterocytes to stem cells serves to couple cell death and division and maintain constant cell number. In enterocytes, the adhesion receptor E-cadherin (E-cad) inhibits stem cell divisions not by binding stem cell E-cad, but by repressing the EGF maturation factor rhomboid to limit secretion of enterocyte EGFs. Conversely, loss of E-cad upon physiological apoptosis derepresses rhomboid, triggering local activation of EGFR in nearby stem cells. EGFR activation induces stem cells to divide, generating new cells to replace apoptotic enterocytes. When enterocyte apoptosis is blocked, stem cells compensate by slowing their divisions. Disrupting E-cad-EGFR feedback inhibition impairs this compensatory response and leads to organ hyperplasia. Our results show that global inhibition of stem cell EGFR is locally relieved when an enterocyte apoptoses. This mechanism couples division and death, ensuring zero-sum cell replacement and constant organ size during renewal.