Assessing at-sea distributions and behaviour of seabirds to identify critical foraging sites and spatial overlap with potential threats is a major step for delineating conservation guidelines. The West African Crested Tern (Thalasseus albididorsalis) is the most abundant breeding tern in West Africa, nesting from Mauritania to Guinea. Its restricted breeding range and exclusive nesting at coastal low-lying areas, place this species at particular risk of losing suitable breeding and resting sites as a consequence of current global changes, namely, sea-level rise. The at-sea distribution of this species is mostly unknown, and therefore, the specific threats faced are still unidentified. Here, we characterize the foraging behaviour and distribution of West African Crested terns breeding at the world’s second-largest colony of the species, in Guinea-Bissau, by tracking 20 individuals. Overall, terns took an average of 2 trips per day, travelling on average 100 km per trip, but often reaching areas up to 120 km from the colony. Shallow waters, usually not exceeding 10 m in depth, and upwelling areas were mostly used as foraging sites. Nocturnal movements, rarely reported on terns, suggest active foraging at night. Key foraging and resting sites were identified, which altogether may regularly hold 2.5–23% of the global breeding population of the West African Crested Tern. These areas are only partly (ca. 50%) covered by the existing marine Important Bird and Biodiversity Area (IBA). Therefore, our results should be considered in any re-evaluation of the IBA borders.