The High Seas, lying beyond the boundaries of nations’ Exclusive Economic Zones, cover the majority of the ocean surface and host roughly two thirds of marine primary production. Yet, only a small fraction of global wild fish catch comes from the High Seas, despite intensifying industrial fishing efforts. The surprisingly small fish catch could reflect economic features of the High Seas - such as the difficulty and cost of fishing in remote parts of the ocean surface - or ecological features resulting in a small biomass of fish relative to primary production. We use the coupled biological-economic model BOATS to estimate contributing factors, comparing observed catches with simulations where: (i) fishing cost depends on distance from shore and seafloor depth; (ii) catchability depends on seafloor depth or vertical habitat extent; (iii) regions with micronutrient limitation have reduced biomass production; (iv) the trophic transfer of energy from primary production to demersal food webs depends on depth; and (v) High Seas biomass migrates to coastal regions. Our results suggest that the most important features are ecological: demersal fish communities receive a large proportion of primary production in shallow waters, but very little in deep waters due to respiration by small organisms throughout the water column. Other factors play a secondary role, with migrations having a potentially large but uncertain role, and economic factors having the smallest effects. Our results stress the importance of properly representing the High Seas biomass in future fisheries projections, and clarify their limited role in global food provision.