•Advanced MRI scans can detect long-term concussion-related brain damage.•Repetitive concussive events can result in lasting functional brain abnormalities.•Minimal microstructural damage was detected in the aging, retired athletes.•Pre-motor cortex, hippocampus dentate gyrus and visual cortex were commonly injured.•Impaired social functioning, emotional well-being, energy, and general health. This brain imaging study examined subjects with a history of repetitive concussive and sub-concussive impacts sustained over the course of their careers in the Canadian Football League (CFL). We hypothesized that microstructural and functional abnormalities, assessed using diffusion tensor imaging (DTI) and resting state functional magnetic resonance imaging (rsfMRI) respectively, would be present in these retired athletes, that are not present in matched controls. Seventeen aging, retired CFL players (aged 58.5±6.2y, ranged 45–66) completed three neuropsychological tests, and had anatomical, diffusion and functional MRI scans performed. Healthy age- and sex-matched control data (n = 2117) were used to develop a subject-specific and region-wise Z-scoring approach. Regional DTI fractional anisotropy (FA) and rsfMRI signal complexity (fractal dimension; FD) Z-score data was further analyzed as a subject-specific total, left, and right injury burden (IB) value for each MRI metric. Microstructural abnormality was detected in 6 of 17 subjects based on DTI FA. The rsfMRI data showed 4 subjects with higher total FDIB, and several regions had Z-score outliers detected in multiple subjects. The right pre-motor cortex, right hippocampus dentate gyrus, and right visual cortex were the most abnormally functioning grey matter brain regions. Total FAIB was negatively correlated with career length, social functioning, and significantly with emotional well-being, and positively correlated with physical health. Total FDIB was negatively correlated with energy and fatigue and general health, and positively correlated with age, career length, and education. This study provides evidence of brain changes years after professional athletes have retired.