The walking gaits of cursorial quadrupedal mammals tend to be highly stereotyped as a four-beat pattern with interspersed periods of double and triple stance, often with double-hump ground reaction force profiles. This pattern has long been associated with high energetic economy, due to low apparent work. However, there are differing ways of approximating the work performed during walking and, consequently, different interpretations of the primary mechanism leading to high economy. A focus on Net Center of Mass (COM) Work led to the claim that quadrupedal walking is efficient because it effectively trades potential and kinetic energy of the COM. Individual Limbs COM Work instead focuses on the ability of the limbs to manage the trajectory of the COM to limit energetic losses to the ground (“collisions”). By focusing on the COM, both these metrics effectively dismiss the importance of rotation of the elongate quadrupedal body. Limb Extension Work considers work required to extend and contract each limb like a strut, and accounts for the work of body pitching. We tested the prescriptive ability of these approximations of work by optimizing them within a quadrupedal model with two approximations of the body as a point-mass or a rigid distributed mass. Perfect potential-kinetic energy exchange of the COM was possible when optimizing Net COM Work, resulting in highly compliant gaits with duty factors close to one, far different than observed mammalian gaits. Optimizing Individual Limbs COM Work resulted in alternating periods of single limb stance. Only the distributed mass model, with Limb Extension Work as the cost, resulted in a solution similar to the stereotypical mammalian gait. These results suggest that maintaining a near-constant limb length, with distributed contacts, are more important mechanisms of economy than either transduction of potential-kinetic energy or COM collision mitigation for quadrupedal walking.