The standard view of embryogenesis is one of cooperation driven by the cells' shared genetics and evolutionary interests. However, numerous examples from developmental biology and agriculture reveal a surprising amount of competition among body cells, tissues, and organs for both metabolic and informational resources. To explain the existence of such competition we had hypothesized that evolution uses limiting “reservoirs” of resource molecules as a communication medium - a global scratchpad, to enable tissues across the body to coordinate growth. Here, we test this hypothesis via an evolutionary simulation of embryogeny in silico. Genomes encode state transition rules for cells, such as proliferation, differentiation, and resource use, enabling virtual embryos to develop a specific large-scale morphology. An evolutionary algorithm operates over the genomes, with fitness defined as a function of specific morphological requirements for the final embryo shape. We found that not only does such an algorithm rapidly discover rules for cellular behavior that reliably make embryos with specific anatomical properties, but that it discovers the strategy of using finite resources to coordinate development. Given the option of using finite or infinite reservoirs (which determine cells’ ability to carry out specific actions), evolution preferentially uses finite reservoirs, which results in higher fitness and increased consistency (without needing direct selection for morphological invariance). We report aspects of anatomical, physiological/transcriptional, and genomic analysis of evolved virtual embryos that help understand how evolution can use competition among genetically identical subunits within a multicellular body to coordinate reliable, complex morphogenesis. Our results suggest that under some conditions, composite multi-scale systems will promote conflict and artificial scarcity for their components.