Humans, like all organisms, are subject to fundamental biophysical laws. Van Valen predicted that, because of zero-sum dynamics, all populations of all species in a given environment flux the same amount of energy on average. Damuth's 'energetic equivalence rule' supported Van Valen's conjecture by showing a trade off between few big animals per area with high individual metabolic rates compared to abundant small species with low energy requirements. We use established metabolic scaling theory to compare variation in densities and individual energy use in human societies to other land mammals. We show that hunter-gatherers occurred at lower densities than a mammal of our size. Most modern humans, in contrast, concentrate in large cities at densities that are up to four orders of magnitude greater than hunter-gatherers yet cities consume up to two orders of magnitude greater energy per capita. Today, cities across the globe flux greater energy than net primary productivity on a per area basis. This is possible through enormous fluxes of energy and materials across urban boundaries to sustain hyper-dense, modern humans. The metabolic rift with nature created by hyper-dense cities supported by fossil fuel energy poses formidable challenges for establishing a sustainable relationship on a rapidly urbanizing, yet finite planet.