Many viruses package their genomes into procapsids using an ATPase machine that is among the most powerful known biological motors. However, how this motor couples ATP hydrolysis to DNA translocation is still unknown. Here, we introduce a model system with unique properties for studying motor structure and mechanism. We describe crystal structures of the packaging motor ATPase domain that exhibit nucleotide-dependent conformational changes involving a large rotation of an entire subdomain. We also identify the arginine finger residue that catalyzes ATP hydrolysis in a neighboring motor subunit, illustrating that previous models for motor structure need revision. Our findings allow us to derive a structural model for the motor ring, which we validate using small-angle X-ray scattering and comparisons with previously published data. We illustrate the model’s predictive power by identifying the motor’s DNA-binding and assembly motifs. Finally, we integrate our results to propose a mechanistic model for DNA translocation by this molecular machine. Many viruses use a molecular motor to pump DNA into a preformed protein shell called the capsid, a process that is essential for the formation of infectious virus particles. The ATPase machine powering this process is the strongest known biological motor. However, the structure and mechanism of this motor are unknown. Here, we derive a structural model of the ATPase assembly using a combination of X-ray crystallography, small-angle X-ray scattering, molecular modeling, and biochemical data. We identify residues critical for ATP hydrolysis and DNA binding, and derive a mechanistic model for the translocation of DNA into the viral capsid. Our studies introduce a model for ATPase assembly and illustrate how DNA is pumped with high force.