Adenosine triphosphate (ATP) production and utilization is critically important for animal development. How these processes are regulated in space and time during tissue growth remains largely unclear. We used a FRET‐based sensor to dynamically monitor ATP levels across a growing tissue, using the Drosophila larval wing disc. Although steady‐state levels of ATP are spatially uniform across the wing pouch, inhibiting oxidative phosphorylation reveals spatial differences in metabolic behavior, whereby signaling centers at compartment boundaries produce more ATP from glycolysis than the rest of the tissue. Genetic perturbations indicate that the conserved Hedgehog signaling pathway can enhance ATP production by glycolysis. Collectively, our work suggests the existence of a homeostatic feedback loop between Hh signaling and glycolysis, advancing our understanding of the connection between conserved developmental patterning genes and ATP production during animal tissue development. Synopsis Morphogen signaling in the developing Drosophila wing can promote adenosine triphosphate (ATP) production from glycolysis upon loss of oxidative phosphorylation (OxPhos). An ATP FRET sensor reveals regional differences in energy metabolism across the wing pouch upon treatment with inhibitors of OxPhos and glycolysis. Regions of high morphogen signaling near compartment boundaries produce more ATP from glycolysis than the rest of the wing pouch, resulting in slower decline of ATP upon OxPhos inhibition. Genetic perturbations indicate that Hh signaling promotes glycolytic ATP production under energy stress. Enhancement of glycolytic ATP production by Hh signaling could preserve important morphogen signaling centers during brief periods of physiologically relevant energy stress, including hypoxia. Morphogen signaling in the developing Drosophila wing can promote adenosine triphosphate production from glycolysis upon loss of oxidative phosphorylation (OxPhos).