BackgroundPoa 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 ofP. annua’sdiploid progenitors,P. infirmaandP. supina,and use multi-omic analyses spanning all three species to better understandP. annua’sevolutionary novelty.ResultsWe find that the diploids diverged from their common ancestor 5.5 – 6.3 million years ago and hybridized to formP. 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 allotetraploidP. annua,we find biased movement of retrotransposons from the larger (A) subgenome to the smaller (B) subgenome. We show thatP. annua’sB subgenome is preferentially accumulating genes and that its genes are more highly expressed. Whole-genome resequencing of several additionalP. annuaaccessions revealed large-scale chromosomal rearrangements characterized by extensive TE-downsizing and evidence to support the Genome Balance Hypothesis.ConclusionsThe divergent evolutions of the diploid progenitors played a central role in conferring ontoP. annuaits 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 thatP. annuauses 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.Supplementary InformationThe online version contains supplementary material available at 10.1186/s12864-023-09456-5.