Predator-prey interactions present a powerful framework for understanding population regulation in natural systems, including the vast and understudied pelagic deep sea. Oceanic squid are among the most abundant and important species groups in this habitat and function as primary prey for the largest marine top predators, deep-diving cetaceans. At the same time, these cryptic animals are highly data deficient. Insight into the dynamics of deep-sea squid populations and the impacts of predation by top-predators is crucial for designing conservation strategies and developing a general theory of deep-sea ecology. Here, we offer fundamental new insights into how individual life history and predation interact to shape population regulation in deep-sea squid. Using empirical data, we develop a size-structured population model for a highly abundant histioteuthid deep-sea squid. We show that population regulation is driven primarily by conditions experienced as paralarvae in the upper water column, where they face intense resource competition. Relaxation of this competition following ontogenetic migration as juveniles drives exponential-like growth curves. Population dynamics exhibit single-cohort cycles, producing regular seasonal patterns in reproduction, even in the absence of any environmental seasonality. Furthermore, we demonstrate that predation by deep-diving cetaceans at different depths can lead to emergent facilitation between top predators. This reveals the complex interdependencies in trophic networks connecting the deep sea with surface waters. Our findings provide critical insights into the ecological functioning of the pelagic deep-sea and their link with surface waters. These insights are urgently needed to better understand and conserve this vast, data-deficient habitat, which endangered deep-diving predators depend on but is under major stress from anthropogenic activities.