Bone strength depends on several material and structural properties, but findings concerning the best predictors of bone mechanical performance are conflicting. The aim of this study was to investigate how a broad set of bone properties in the proximal femur are influenced by age and hormonal status, and how these properties together determine bone strength. Twenty-five Wistar rats were ovariectomized (OVX, n = 13) or sham operated (SHAM, n = 12) at 5 months of age, and killed after 9 months. Another group of rats was killed at 5 months as baseline control (BSL, n = 7). At sacrifice, serum 17β-estradiol and bone turnover marker concentrations were determined in the serum. Both femurs were collected for assessment of trabecular microarchitecture, femoral neck geometry, radiographic absorptiometry, calcium and phosphate content, and biomechanical properties. While stiffness was mostly associated with proximal femur trabecular microarchitecture and mineralization degree, bone strength was mostly linked to bone size and femoral neck geometry, which predicted almost 50% of its variance. Despite the decrease in cortical and trabecular bone as well as in mineralization degree following estrogen loss, bone strength was not reduced in OVX animals compared to BSL or sham-operated rats. This was due to a change in femoral neck geometry as well as to an increase in femur size in OVX, which apparently compensated their lower bone volume and mineral content, thereby preserving bone strength. Estrogen loss leads to a deterioration of bone tissue quality, but bone strength was preserved at the expense of geometric adaptations.