Background: Poa annua (annual bluegrass) is an allotetraploid turfgrass, an agronomically significant weed, and one of the most widely dispersed plant species on earth. Here, we report the chromosome-scale genome assemblies of P. annua’s diploid progenitors, P. infirma and P. supina, and use multi-omic analyses spanning all three species to better understand P. annua’s evolutionary novelty. Results: We find that the diploids diverged from their common ancestor 5.5 – 6.3 million years ago and hybridized to form P. annua ≤ 50,000 years ago. The diploid genomes are similar in chromosome structure and most notably distinguished by the divergent evolutionary histories of their transposable elements, leading to a 1.7 × difference in genome size. In allotetraploid P. annua, we find biased movement of retrotransposons from the larger (A) subgenome to the smaller (B) subgenome. We show that P. annua’s B subgenome is preferentially accumulating genes and that its genes are more highly expressed. Whole-genome resequencing of several additional P. annua accessions revealed large-scale chromosomal rearrangements characterized by extensive TE-downsizing and evidence to support the Genome Balance Hypothesis. Conclusions: The divergent evolutions of the diploid progenitors played a central role in conferring onto P. annua its remarkable phenotypic plasticity. We find that plant genes (guided by selection and drift) and transposable elements (mostly guided by host immunity) each respond to polyploidy in unique ways and that P. annua uses whole-genome duplication to purge highly parasitized heterochromatic sequences. The findings and genomic resources presented here will enable the development of homoeolog-specific markers for accelerated weed science and turfgrass breeding.

Poa annua L. (annual bluegrass) is a remarkably versatile grass species with biotypes ranging from perennial to annual. Despite its recent evolutionary origins, Poa annua can be found as an invasive weed on all seven continents of the globe including extremely inhospitable locations such as Mount Kilimanjaro and the Antarctic mainland. The molecular mechanisms underlying Poa annua versatility are unresolved but thought to relate to its neoallopolyploid origin and influence diverse molecular responses ranging from DNA methylation to chromosomal architecture. Fluorescence in situ hybridization (FISH) karyotyping of 5S rDNA loci added further evidence for Poa infirma Kunth. (weak bluegrass) and Poa supina Schrad. (supina bluegrass) as the progenitor species of Poa annua while results of 45S rDNA were less clear and possibly suggest that large‐scale variation in chromosomal architecture might have occur between individual Poa annua genotypes. At the methylation level, abiotic stress was observed to induce global DNA methylation, and methylation in the progeny of stressed plants remained slightly elevated, suggesting partial heritability of the methylation landscape acquired through abiotic stress on the parents. Further, the progeny of mowed clones had 37% reduced shoot area when compared with the progeny of unmowed clones across eight genotypes, suggesting that the altered phenotype is non‐Mendelian inherited. Poa annua plasticity and transgenerational inheritance is correlated with increased DNA methylation at the global level but causality needs experimental validation. These results suggest that Poa annua plastic phenotype is matched by genetic and epigenetic plasticity.