Purpose Asymmetrical loading patterns are commonplace in football sports. Our aim was to examine the influence of training age and limb function on lower-body musculoskeletal morphology. Methods Fifty-five elite football athletes were stratified into less experienced (≤3 yr; n = 27) and more experienced (>3 yr; n = 28) groups by training age. All athletes underwent whole-body dual-energy x-ray absorptiometry scans and lower-body peripheral quantitative computed tomography tibial scans on the kicking and support limbs. Results Significant interactions between training age and limb function were evident across all skeletal parameters (F16, 91 = 0.182, P = 0.031, Wilks Λ = 0.969). Asymmetries between limbs were significantly larger in the more experienced players than the less experienced players for tibial mass (P ≤ 0.044, d ≥ 0.50), total cross-sectional area (P ≤ 0.039, d ≥ 0.53), and stress-strain indices (P ≤ 0.050, d ≥ 0.42). No significant asymmetry was evident for total volumetric density. More experienced players also exhibited greater lower-body tibial mass (P ≤ 0.001, d ≥ 1.22), volumetric density (P ≤ 0.009, d ≥ 0.79), cross-sectional area (P ≤ 0.387, d ≥ 0.21), stress-strain indices (P ≤ 0.012, d ≥ 0.69), fracture loads (P ≤ 0.018, d ≥ 0.57), and muscle mass and cross-sectional area (P ≤ 0.016, d ≥ 0.68) than less experienced players. Conclusions Asymmetries were evident in athletes as a product of limb function over time. Chronic exposure to routine high-impact gravitational loads afforded to the support limb preferentially improved bone mass and structure (cross-sectional area and cortex thickness) as potent contributors to bone strength relative to the high-magnitude muscular loads predominantly afforded to the kicking limb.