show Abstracthide AbstractCnidaria (sea anemones, jellyfish, corals and hydra) form a close outgroup to Bilateria, and the sea anemone Nematostella vectensis has emerged as a slow evolving model, illuminating characteristics of the most recent common ancestor to Bilateria, which diverged near the Cambrian explosion. Using long read sequencing and high throughput chromosome conformation capture, we generated high quality chromosome-level assemblies of N. vectensis and the closely related edwardsiid sea anemone, Scolanthus callimorphus. In both cases we find a robust set of 15 chromosomes comprising a stable linkage group detectable within all major clades of sequenced cnidarian genomes and demonstrate remarkable chromosomal conservation with chordates. Unlike in Bilateria, extended Hox and NK gene clusters are chromosomally linked but do not retain a tight spatial conservation. Accordingly, we also observe a lack of evidence for topologically associated domains, which have been implicated in the evolutionary pressure to retain tight microsyntenic gene clusters. We also uncover ultra-conserved noncoding elements at levels previously undetected in non-chordate lineages. Both genomes are accessible through an actively updated genome browser and database at https://simrbase.stowers.org.