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Abstract When studying bone fragility diseases, it is difficult to identify which factors reduce bone’s resistance to fracture because these diseases alter bone at many length scales. Here, we investigate the contribution of nanoscale collagen behavior on macroscale toughness and microscale toughening mechanisms using a bovine heat-treatment fragility model. This model is assessed by developing an in situ toughness testing technique for synchrotron radiation micro-computed tomography to study the evolution of microscale crack growth in 3D. Low-dose imaging is employed with deep learning to denoise images while maintaining bone’s innate mechanical properties. We show that collagen damage significantly reduces macroscale toughness and post-yield properties. We also find that bone samples with a compromised collagen network have reduced amounts of crack deflection, the main microscale mechanism of fracture resistance. This research demonstrates that collagen damage at the nanoscale adversely affects bone’s toughening mechanisms at the microscale and reduces the overall toughness of bone.