Mild traumatic brain injury is widely regarded as a misnomer: it is globally a major cause of disability and is hypothesized as a potential causal factor in subsequent neurodegeneration. Commonly arising in sport, mounting evidence of varying degrees of cognitive impairment in retired athletes exposed to repeated concussions motivates close examination of its cumulative effects on the brain. Studying a cohort of 125 retired athletes with a mean of 11 reported concussions and 36 matched controls with none, here we evaluated whole-brain volumetric and subcortical morphological effects with Bayesian regression models and functional connectivity effects with network-based statistics. Estimates of potential cognitive impact were derived from meta-analytic functional mapping based on 13,459 imaging studies. Across the array of brain structural and functional effects identified, regions significantly lower in volume in the concussed group included, in order of greatest effect size, the middle frontal gyrus, hippocampus, supramarginal gyrus, temporal pole, and inferior frontal gyrus. Conversely, brain regions significantly larger within the athlete group included, in order of greatest effect size, the hippocampal and collateral sulcus, middle occipital gyrus, medial orbital gyrus, caudate nucleus, lateral orbital gyrus, and medial segment to the postcentral gyrus (all significant with 95% Bayesian credible interval). Subcortical morphology analysis corroborated these findings, revealing a significant, age-independent relationship between inward deformation of the hippocampus and the number of concussions sustained (corrected- p<0.0001). Functional connectivity analyses revealed a distinct brain network with significantly increased edge strength in the athlete cohort comprising 150 nodes and 400 edges (corrected-p=0.02), with the highest degree nodes including the pre-central and post-central gyri and right insula. The functional communities of the greatest eigenvector centralities corresponded to motor domains. Numerous edges of this network strengthened in athletes were significantly weakened with increasing bouts of concussion, which included disengagement of the frontal pole, superior frontal, and middle frontal gyri (p=0.04). Aligned to meta-analytic neuroimaging data, the observed changes suggest possible functional enhancement within the motor, sensory, coordination, balance, and visual processing domains in athletes, attenuated by concussive head injury with a negative impact on memory and language. That such changes are observed many years after retirement from impact sport suggests strong repetition effects and/or underpinning genetic selection factors. These findings suggest that engagement in sport may benefit the brain across numerous domains, but also highlights the potentially damaging effects of concussive head injury.