The study of the evolution of brain-behavior relationships concerns understanding the causes and repercussions of cross- and within-species variability. Understanding such variability is a main objective of evolutionary and cognitive neuroscience, and it may help explaining the appearance of psychopathological phenotypes. Although the brain evolution is related to the progressive action of selection and adaptation through multiple paths (e.g., mosaic vs. concerted evolution, metabolic vs. structural and functional constraints), a coherent, integrative framework is needed to combine evolutionary paths and neuroscientific evidence. Here, we review the literature on evolutionary pressures focusing on structural-functional changes and developmental constraints. Taking advantage of progresses in neuroimaging and cognitive neuroscience, we propose a twofold model of brain evolution. Within this model, global and local trajectories imply rearrangements of neural subunits and subsystems as well as of behavioral repertoires of a species, respectively. We incorporate these two processes in a game in which the global trajectory shapes the structural-functional neural substrates (i.e., players), while the local trajectory shapes the behavioral repertoires (i.e., stochastic payoffs).