Double-stranded DNA viruses, including most bacteriophages and mammalian herpesviruses, package their genomes into a pre-formed protein capsid during their self-assembly. DNA is compacted to near-crystalline densities at the end of packaging. This remarkable mechanical task is performed by a powerful ATP-driven molecular machine known as the packaging motor. Bacteriophage Phi29, a model system for studying DNA packaging, has a 19.3-kbp genome and its packaging motor is composed of a connector, an RNA scaffold, and a pentameric ring ATPase. Ring ATPases of the ASCE superfamily perform a variety of cellular functions. An important question about the operation of these molecular machines is how the ring subunits coordinate their chemical and mechanical transitions. Here we present the first comprehensive mechanochemical characterization of a homomeric ring ATPase - Phi29 gp16 - which translocates dsDNA in cycles composed of alternating dwells and bursts. We use high-resolution optical tweezers to determine the effect of nucleotide analogs on the cycle. We find that ATP hydrolysis occurs sequentially during the burst and that ADP release is interlaced with ATP binding during the dwell, revealing a high degree of coordination among ring subunits. Moreover, we show that the motor displays an unexpected division of labor: although all subunits of the homo-pentamer bind and hydrolyze ATP during each cycle, only four participate in translocation whereas the remaining subunit plays an ATP-dependent regulatory role. Several viral packaging motors have been shown to slow down as the capsid fills up with DNA, but it remains unclear how the packaging velocity is regulated. Here we use high-resolution optical tweezers to monitor the base-pair-scale packaging dynamics at various degrees of capsid filling. By comparing the burst duration at various degrees of capsid filling and different external forces, we estimate an internal force of ~20 pN at 100% filling, much lower than the motor's stall force. We find that the motor's step size is continuously modulated by capsid filling, in quantitative agreement with measurements of DNA rotation by the Phi29 packaging motor. In addition, we find the motor switches on and off at high filling by entering into long-lived pauses, which may allow DNA relaxation within the capsid. Together, our results reveal that the motor is not passively stalled by a large internal force at high filling as suggested by previous models. Instead, the motor is actively throttled down via several mechanisms in response to DNA encapsidation. The intricate crosstalk between the motor and the capsid plays a key role in orchestrating the molecular events leading to packaging termination and virus maturation, and may represent a general design principle shared by different viruses.