Applications of graph theory to the connectome have inspired several models of how neural signaling unfolds atop its structure. Analytic measures derived from these communication models have mainly been used to extract global characteristics of brain networks, obscuring potentially informative inter-regional relationships. Here we develop a simple standardization method to investigate polysynaptic communication pathways between pairs of cortical regions. This procedure allows us to determine which pairs of nodes are topologically closer and which are further than expected on the basis of their degree. We find that communication pathways delineate canonical functional systems. Relating nodal communication capacity to meta-analytic probabilistic patterns of functional specialization, we also show that areas that are most closely integrated within the network are associated with higher order cognitive functions. We find that these regions’ proclivity towards functional integration could naturally arise from the brain’s anatomical configuration through evenly distributed connections among multiple specialized communities. Throughout, we consider two increasingly constrained null models to disentangle the effects of the network’s topology from those passively endowed by spatial embedding. Altogether, the present findings uncover relationships between polysynaptic communication pathways and the brain’s functional organization across multiple topological levels of analysis and demonstrate that network integration facilitates cognitive integration. Author Summary Several mathematical models describe how neural signaling unfolds atop the structure of the brain. These communication models have mainly been used to characterize brain networks at a global scale. Here, using a simple standardization procedure, we benchmark inter-regional measures of communication capacity to determine which pairs of brain regions show a higher or lower propensity to communicate than expected by chance. We identify relationships between communication pathways and the brain’s functional organization across multiple network levels and show that network integration facilitates cognitive integration. Throughout, we consider the effect of spatial proximity on inter-regional communication relationships.