Chromosome conformation capture (3C/Hi-C)-based methods have been used extensively to probe the average 3D organization of genomes, revealing fundamental aspects of chromosome dynamics. However, when applied to prokaryotic and archaeal species the current protocols are expensive, inefficient, and limited in their resolution. We developed a cost-effective approach that allows the exploration of bacterial and archaeal chromosome conformations at the gene or operon level. We applied it to the Euryarchaea H. volcanii, Hbt. salinarum and T. kodakaraensis. We generated genome-wide contact maps at a resolution of up to 1kb, allowing us to further explore the diversity of chromosome folding in this kingdom. We show that, in contrast to Crenarchaea, these Euryarchaea lack (active and inactive) compartment-like structures, and instead resemble the architecture of bacterial chromosomes. The genomes also display sub-Mb domains and DNA loops. In H. volcanii, these structures are regulated by both transcription and the archaeal SMC protein, further supporting the ubiquitous role of these mechanisms in shaping the higher-order organization of genomes in all kingdoms.