Multi-subunit SMC ATPases control chromosome superstructure and DNA topology, presumably by DNA translocation and loop extrusion. Chromosomal DNA is entrapped within the tripartite SMCkleisin ring. Juxtaposed SMC heads ("J heads") or engaged SMC heads ("E heads") split the SMCkleisin ring into "S" and "K" sub-compartments. Here, we map a DNA-binding interface to the S compartment of E heads SmcScpAB and show that head-DNA association is essential for efficient DNA translocation and for traversing highly transcribed genes in Bacillus subtilis. We demonstrate that in J heads, SmcScpAB chromosomal DNA resides in the K compartment but is absent from the S compartment. Our results imply that the DNA occupancy of the S compartment changes during the ATP hydrolysis cycle. We propose that DNA translocation involves DNA entry into and exit out of the S compartment, possibly by DNA transfer between compartments and DNA segment capture.