The measures of bone mass and architecture need to be supplemented with physicochemical and compositional measures for better assessment of fracture risk. In the current studies, we investigated the effects of physicochemical properties of mineral crystals on tissue and organ-level mechanical function of aging rat cortical bone. Our hypothesis was that age-related changes in physicochemical properties of mineral crystals are related to impaired elastic deformability of cortical bone tissue. Raman microspectroscopy was used to investigate the age-related changes in mineralization (relative amounts of mineral and organic matrix), the substitution of carbonate ions in phosphate positions (type-B carbonate substitution) and mineral crystallinity (the orderliness of crystal lattice) of femurs from young adult (3-month old), middle-aged (8-month old) and aged (24-month old) female Sprague–Dawley rats. Cross-sectional properties, the area and the moment of inertia at the mid-diaphysis, were histomorphometrically quantified and the elastic deformation capacity of femurs was quantified via three-point bending tests. It was observed that the elastic deformation capacity of aged rats was significantly impaired both at the tissue and the organ levels with increasing age. In parallel with this impairment in the elastic deformability and in support of our hypothesis, we found that increasing mineralization, increasing crystallinity and increasing type-B carbonate substitution were significantly correlated with decreasing elastic deformation capacity with age. We conclude that the measure of bone mass needs to be supplemented with measures reflecting the physicochemical status of mineral crystals for improved assessment of fracture susceptibility.