Compared to their domesticated annual counterparts, undomesticated perennial plant genomes often exhibit high levels of genome duplication followed by neofunctionalization. Further, their long-life spans allow for sustained interactions with endophytic microbes leading to high levels of horizontal DNA transfer events that results in genetic novelty. Using high-performance computing and data-driven approaches incorporation >1,500 Whole Genome Resequenced genotypes, >4,000 multi-tissue transcriptomes and thousands of phenotypic datasets, we provide examples of genetic novelty ranging from transcription regulation of cell wall biosynthesis, defense signaling, photosynthesis efficiency, biotic and abiotic stress tolerance, all of which violate canonical expectations.