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Abstract Understanding how evolution shapes genetic networks to create new developmental forms is a central question in biology. Flowering shoot (inflorescence) architecture varies significantly across plant families and is a key target of genetic engineering efforts in many crops^1–4. Asteraceae (sunflower family), comprising 10% of flowering plants, all have capitula, a novel inflorescence that mimics a single flower^5,6. Asteraceae capitula are highly diverse but are thought to have evolved once via unknown mechanisms^7,8. During capitulum development, shoot stem cells undergo prolonged proliferation to accommodate the formation of intersecting spirals of flowers (florets) along the disk-shaped head^9,10. Here we show that capitulum evolution paralleled decreases in CLAVATA3 (CLV3) peptide signaling, a conserved repressor of stem cell proliferation. We trace this to novel amino acid changes in the mature CLV3 peptide which decrease receptor binding and downstream transcriptional outputs. Using genetically tractable Asteraceae models, we show that reversion ofCLV3to a more active form impairs Asteraceae stem cell regulation and capitulum development. Additionally, we trace the evolution ofCLV3and its receptors across the Asterales allowing inferences on capitulum evolution within this lineage. Our findings reveal novel mechanisms driving evolutionary innovation in plant reproduction and suggest new approaches for genetic engineering in crop species.