In many animal systems, the local activation of patterning signals in spatially confined regions (organizers) is crucial for promoting the growth of developing organs. Nevertheless, how organizers are set up and how their activity influences global organ growth remains poorly understood. In the Drosophila eye, local Notch activation establishes a conserved dorsal-ventral organizer that promotes growth. The dorsal selector Iroquois complex defines the position of the organizer at the mid-first instar, and through its ligand, unpaired, the Janus kinase (JAK)/signal transducers and activator of transcription (STAT) pathway is thought to mediate global growth downstream of the organizer. However, here we show that the unpaired/JAK/STAT pathway is actually a fundamental element in the spatial control of the organizer, upstream from Notch activation. Furthermore, we identify four-jointed, a target of the Fat and Hippo tumour-suppressor pathways, as a mediator of the growth controlled by the organizer. These findings redefine the process of organizer formation and function, and they identify four-jointed as a regulatory node, integrating multiple growth-control pathways.