The cortical connections of the human hippocampal memory system are fundamental to understanding its operation in health and disease, especially in the context of the great development of the human cortex. The functional connectivity of the human hippocampal system was analyzed in 172 participants imaged at 7T in the Human Connectome Project. The human hippocampus has high functional connectivity not only with the entorhinal cortex, but also with areas that are more distant in the ventral ‘what’ stream including the perirhinal cortex and temporal cortical visual areas. Parahippocampal gyrus TF in humans has connectivity with this ventral ‘what’ subsystem. Correspondingly for the dorsal stream, the hippocampus has high functional connectivity not only with the presubiculum, but also with areas more distant, the medial parahippocampal cortex TH which includes the parahippocampal place or scene area, the posterior cingulate including retrosplenial cortex, and the parietal cortex. Further, there is considerable cross connectivity between the ventral and dorsal streams with the hippocampus. The findings are supported by anatomical connections, which together provide an unprecedented and quantitative overview of the extensive cortical connectivity of the human hippocampal system that goes beyond hierarchically organised and segregated pathways connecting the hippocampus and neocortex, and leads to new concepts on the operation of the hippocampal memory system in humans.