Plastic phenotypes are important biological adaptations, yet their evolution and genomic basis remains insufficiently unexplored. This study examines the origin of an inducible defensive structure, the helmet, that emerged during evolution of a novel morphotype in the freshwater microcrustacean Daphnia sinensis. This specific morphotype exhibits consitutively expressed pointed head shape as a juvenile, and forms conspicuous retrocurved helmets in response to infochemicals of the predatory cladoceran Leptodora. Our genomic analyses, focusing on single-nucleotide and genome structural variation, indicate monophyletic origin of this morphotype, which apparently emerged following a pond-to-lake habitat shift. The ancestral round-headed morphotype of D. sinensis lives in pond habitats without Leptodora and apparently lacks ability to form large inducible helmets. The divergence of the two morphotypes is characterized by signals of positive selection and extensive chromosome structural changes. A signal of hard selective sweep is particularly strong in the tightly linked ISM1 and TM2D2 genes, both involved in morphogenesis, but with contrasting level of divergence between morphotypes. ISM1 differs in coding regions and amino acid sequences, indicating protein-level changes; TM2D2 differences primarily involve regulatory regions, as confirmed by different level of expression of this gene between morphotypes despite shared protein sequences. Daphnia knockout mutants for TM2D2 or ISM1, generated from a helmet-forming clone using CRISPR-Cas9, exhibit much reduced plastic formation of the helmet, demonstrating the polygenic control of this adaptive trait and large effect sizes of the respective genes. Our study characterizes the evolutionary and genetic basis of a classic example of an adaptive plastic trait.