For a terrestrial animal to move in the complex natural environment, the limb muscles must modulate force and work performance to meet changing mechanical requirements; however, it is not clear whether this is accomplished via a collective shift in function by all limb muscles, or a division of labor among limb muscles. Do muscles differ in their ability to modulate force-length contractile function to meet the mechanical demands of different locomotor tasks? We explore this question by examining the in vivo force-length performance of the guinea fowl Numida meleagris lateral gastrocnemius (LG) and digital flexor-IV (DF-IV), during level and incline locomotion. During level locomotion, the LG and DF-IV exhibit differing muscle fascicle strain patterns: the LG shortens by 10-15% while developing force, whereas the DF-IV undergoes a stretch-shorten cycle with large strain amplitudes and small net strains of 1-8%. Furthermore, the DF-IV operates at higher muscle stresses (92-130 kPa, compared to 23-39 kPa for LG) and possesses a longer tendon, which allows the DF-IV tendon to recover greater elastic energy than the LG tendon. During incline locomotion, these muscles contribute only one-third of the energy expected for their mass, with the DF-IV exhibiting high stride-to-stride variability in work output. While the stretch-shorten cycle of the DF-IV muscle may allow more economic force production, it also leads to large changes in work output with small changes in the relative timing of force and strain. Thus, while the primary determinants of LG work are net strain and mean force, the primary determinant of DF-IV work is the phase relationship between force and strain. Our results suggest that, in addition to influencing a muscle's mechanical performance during steady level locomotion, morphology also affects its capacity and mechanism for altering work output for different locomotor tasks.