Magnetic resonance imaging (MRI) enables accurate in vivo quantification of human muscle volumes, which can be used to estimate subject-specific muscle force capabilities. An important consideration is the amount of contractile and non-contractile tissue in the muscle compartment, which will influence force capability. We quantified age-related differences in the proportion and distribution of contractile and non-contractile tissue in the dorsiflexor and plantar flexor (soleus, and medial and lateral heads of gastrocnemius) muscles, and examined how well these volumes can be estimated from single MRI cross-sections. Axial MRIs of the left leg for 12 young (mean age 27 years) and 12 older (72 years) healthy, active adults were used to compute muscle volumes. Contractile tissue distribution along the leg was characterized by mathematical functions to allow volume prediction from single-slice cross-sectional area (CSA) measurements. Compared to young, older adults had less contractile volume and a greater proportion of non-contractile tissue. In both age groups the proportion of non-contractile increased distally, with the smallest proportion near the maximum compartment CSA. A single CSA measurement predicted contractile volume with 8–11% error, with older adults in the higher end of this range. Using multiple slices improved volume estimates by roughly 50%, with average errors of about 3–4%. These results demonstrate significant age-related differences in non-contractile tissue for the dorsiand plantar flexor muscles. Although estimates of contractile volume can be obtained from single CSA measurements, multiple slices are needed for increased accuracy due to inter individual variations in muscle volume and composition.