Background <p>Recent advances in assemblies of nearly gap-free, high-quality genomes have enabled detailed analysis of centromeres in large and highly repetitive crop genomes. Here, we analyze the centromeres of hexaploid oat (<i>Avena sativa</i>) and its tetraploid (<i>Avena insularis</i>) and diploid relatives (<i>Avena longiglumis</i>, <i>Avena atlantica</i> and <i>Avena eriantha</i>).</p> Results <p>Avena centromeres are largely composed of retrotransposons belonging to three families, <i>RLG_Ava</i>, <i>RLG_Cereba</i> and <i>RLG_Beth</i>. Comparative analysis of retrotransposon populations reveals striking differences in centromere composition and architecture among the A, C and D subgenome lineages. We identify distinct profiles of transposable element bursts for these lineages, including the emergence and loss of retrotransposon families and subfamilies. Furthermore, we identify multiple inversions within centromeric regions of <i>Avena sativa</i> and retrace species divergences and polyploidization events in the <i>Avena</i> genus. Despite their close evolutionary relationships, our data show that the studied species exhibit rapid and divergent evolution of centromere architectures, for example through the spread of novel satellite repeats or activity bursts of different retrotransposon families and subfamilies. Additionally, we find that <i>RLG_Ava</i> and <i>RLG_Cereba</i> retrotransposons have been coexisting and possibly competing for the centromeric “niche” since the emergence of the Poaceae.</p> Conclusions <p>Our comparative analyses provide detailed insight into centromere evolution across the <i>Avena</i> genus and reveal that composition and architecture of centromeres can vary greatly even between closely related species and different ploidy levels. Our findings emphasize the need for extended analyses of large genome species to improve our understanding of centromere evolution.</p>