Female reproduction comes at great expense to energy metabolism compensated by extensive organ adaptations including intestinal size. Upon mating, Drosophila ovaries release the steroid hormone Ecdysone that stimulates a 30% net increase of absorptive epithelium by intestinal stem cell (ISC) divisions. Here, we uncover the transcription factor crooked legs (crol) as intraepithelial coordinator of Ecdysone-induced ISC mitosis by establishing Rapport, the first spatiotemporally-controlled dual expression and tracing system for the analysis of paracrine effects on ISC behaviour. Rapport tracing revealed that Ecdysone-induced Crol controls mitogenic Wnt/wg-ligand release from epithelial enterocytes towards ISC, which is counterbalanced by Crol-repression of string/CDC25 and Cyclin-B directly in ISC. Rapport-based ISC tumours confirm paracrine stimulation through the Ecdysone-Crol-Wg axis on mitotic behaviour. Finally, mathematical modelling corroborates increasing enterocyte numbers and Wnt/wg-degradation to set a stable post-mating intestinal size. Together, our findings provide insights into complex endocrine growth control mechanisms during mating-induced adaptations and gastrointestinal cancer.