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Summary Smc/ScpAB promotes chromosome segregation in prokaryotes, presumably by compacting and resolving nascent sister chromosomes. The underlying mechanisms, however, are poorly understood. Here, we investigate the role of the Smc ATPase activity in the recruitment of Smc/ScpAB to the Bacillus subtilis chromosome. We demonstrate that targeting of Smc/ScpAB to ParB/parS loading sites is strictly dependent on engagement of Smc head domains and relies on an open organization of the Smc coiled coils. We find that dimerization of the Smc hinge domain stabilizes closed Smc rods and hinders head engagement as well as chromosomal targeting. Conversely, the ScpAB sub-complex promotes head engagement and Smc rod opening and thereby facilitates recruitment of Smc to parS sites. Upon ATP hydrolysis, Smc/ScpAB is released from loading sites and relocates within the chromosome—presumably through translocation along DNA double helices. Our findings define an intermediate state in the process of chromosome organization by Smc., Graphical Abstract, Highlights • ATP-dependent head engagement is required for chromosomal targeting of Smc/ScpAB • ATP-dependent head engagement drives coiled-coil opening of Smc in vivo • Targeting of Smc/ScpAB to parS/ParB requires the head-proximal coiled coil of Smc • Hinge dimerization antagonizes head engagement, coiled-coil opening, and targeting, Smc/ScpAB is an important chromosome-organizing machine in bacteria. Minnen et al. show that targeting of Smc/ScpAB to chromosomal parS/ParB sites requires ATP-dependent engagement of Smc heads, which promotes disengagement of the Smc coiled coils and drives the complex into a targeting-competent open conformation.