Genome packaging is a fundamental process in a viral life cycle and a prime target of antiviral drugs.Herpesviruses use an ATP-driven packaging motor/terminase complex to translocate and cleave concatemeric dsDNA into procapsids but its molecular architecture and mechanism are unknown.We report atomic structures of a herpesvirus hexameric terminase complex in both the apo and ADP-BeF3-bound states.Each subunit of the hexameric ring comprises three components—the ATPase/terminase pUL15 and two regulator/fixer proteins,pUL28 and pUL33—unlike bacteriophage terminases.Distal to the nuclease domains,six ATPase domains form a central channel with conserved basicpatches conducive to DNA binding and trans-acting arginine fingers are essential to ATP hydrolysis and sequential DNA translocation.Rearrangement of the nuclease domains mediated by regulatory domains converts DNA translocation mode to cleavage mode.Our structures favor a sequential revolution model for DNA translocation and suggest mechanisms for concerted domain rearrangements leading to DNA cleavage.