Although originally primarily a system for functional biology, the thale cress Arabidopsis thaliana has, owing to its broad geographical distribution and adaptation to diverse abiotic and biotic environments, developed into a powerful model in population genomics. Here, we present chromosome-level genome assemblies of 69 diverse accessions located across the global species range. We found that genomic co-linearity is very conserved, even among geographically and genetically distant accessions. Along chromosome arms, megabase-scale rearrangements are rare, typically present only in a single accession. This indicates that the highly re-arranged karyotype of Arabidopsis thaliana (as compared to other Brassicaceae species), is quasi-fixed and that rearrangements in chromosome arms are counter-selected. In contrast, centromeric regions show much higher structural dynamics, and divergences in core centromeres account for most of the variation in genome size. Pan-genome analyses of the gene space uncovered 32,986 distinct gene families, 60% being present in all accessions and 40% appearing to be dispensable, including 18% private to a single accession, indicating unexplored genic diversity. The availability of 69 new Arabidopsis thaliana high-quality genome assemblies will empower future genetic research.