Geometry plays an important role in intervertebral disc (IVD) mechanics. Previous computational studies have found a link between IVD geometry and stiffness. However, few experimental studies have investigated this link, possibly due to difficulties in non-destructively quantifying internal geometric features. Recent advances in ultra-high resolution MRI provides the opportunity to visualise IVD features in unprecedented detail. This study aimed to quantify 3D human IVD geometries using 9.4 T MRIs and to investigate correlations between geometric variations and IVD stiffness. Thirty human lumbar motion segments (fourteen non-degenerate and sixteen degenerate) were scanned using a 9.4 T MRI and geometric parameters were measured. A 1kN compressive load was applied to each motion segment and stiffness was calculated. Degeneration caused a reduction (p < 0.05) in IVD height, a decreased nucleus-annulus area ratio, and a 1.6 ± 3.0 mm inward collapse of the inner annulus. The IVD height, anteroposterior (AP) width, lateral width, cross-sectional area, nucleus-annulus boundary curvature, and nucleus-annulus area ratio had a significant (p < 0.05) influence on IVD stiffness. Linear relationships (p < 0.05, r > 0.47) were observed between these geometric features and IVD compressive stiffness and a multivariate regression model was generated to enable stiffness to be predicted from features observable on clinical imaging (stiffness, N/mm = 6062 – (61.2 × AP width, mm) – (169.2 × IVD height, mm)). This study advances our understanding of disc structure–function relationships and how these change with degeneration, which can be used to both generate and validate more realistic computational models.