The connections that link neurons within as well as between cerebral cortical areas form a multi-scale structural network for communication in the brain. Which principles underlie the organisation of this complex network? We addressed this question by systematically investigating the relation of essential features of cortico-cortical connections, such as their presence or absence as well as patterns of laminar projection origins and terminations, to fundamental structural parameters of cortical areas, such as their distance, similarity in cortical cytoarchitecture as defined by cortical lamination or neuronal density, and similarity in further macroscopic and microscopic morphological features. These systematic analyses demonstrate the presence of an architectural type principle. Across different species (mouse, cat, macaque monkey and human) and different cortices, the essential features of cortico-cortical connections vary consistently and strongly with the cytoarchitectonic similarity of cortical areas. By contrast, such relations were not found as consistently in multivariate analyses for distance, similarity of cortical thickness or cellular morphological features. The presence of the architectonic type principle across mammalian brains allows direct cross-species predictions of the existence and laminar patterns of projections, including for the human brain, where such data are not directly available experimentally. Moreover, intrinsic brain architecture as characterised by architectural type and neural density also accounts for cellular neuronal features, such as cell size or shape. Thus, these findings illuminate a general principle of neural wiring and integrate cortical connectivity and architecture across scales of organisation, with implications for models of cortical physiology as well as developmental mechanisms.