Ultrashort echo time (UTE) magnetic resonance imaging (MRI) measures proton signals in cortical bone from two distinct water pools, bound water, or water that is tightly bound to bone matrix, and pore water, or water that is freely moving in the pore spaces in bone. By isolating the signal contribution from the pore water pool, UTE biomarkers can directly quantify cortical bone porosity in vivo. The Porosity Index (PI) is one non-invasive, clinically viable UTE-derived technique that has shown strong associations in the tibia with μCT porosity and other UTE measures of bone water. However, the efficacy of the PI biomarker has never been examined in the proximal femur, which is the site of the most catastrophic osteoporotic fractures. Additionally, the loads experienced during a sideways fall are complex and the femoral neck is difficult to image with UTE, so the usefulness of the PI in the femur was unknown. Therefore, the aim of this study was to examine the relationships between the PI measure in the proximal cortical shaft of human cadaveric femora specimens compared to (1) QCT-derived bone mineral density (BMD) and (2) whole bone stiffness obtained from mechanical testing mimicking a sideways fall. Fifteen fresh, frozen whole cadaveric femora specimens (age 72.1 ± 15.0 years old, 10 male, 5 female) were scanned on a clinical 3-T MRI using a dual-echo UTE sequence. Specimens were then scanned on a clinical CT scanner to measure volumetric BMD (vBMD) and then non-destructively mechanically tested in a sideways fall configuration. The PI in the cortical shaft demonstrated strong correlations with bone stiffness (r = −0.82, P = 0.0014), CT-derived vBMD (r = −0.64, P = 0.0149), and with average cortical thickness (r = −0.60, P = 0.0180). Furthermore, a hierarchical regression showed that PI was a strong predictor of bone stiffness which was independent of the other parameters. The findings from this study validate the MRI-derived porosity index as a useful measure of whole-bone mechanical integrity and stiffness.