Significance Global vessel traffic is increasing alongside world economic growth. The potential for rising lethal ship strikes on endangered species of marine megafauna, such as the plankton-feeding whale shark, remains poorly understood since areas of highest overlap are seldom determined across an entire species range. Here we show how satellite tracking whale sharks and large vessel movements globally provides a means to localize high-overlap areas and to determine how collision risk changes in time. Our results point to potential high levels of undetected or unreported ship strikes, which may explain why whale shark populations continue to decline despite protection and low fishing-induced mortality. Collision mitigations in high-collision-risk areas appear necessary to help conserve this iconic species.