Simplifying complex species interactions can facilitate tracking and predicting functional responses to ecological stressors. This is important for highly migratory pelagic predators, exploiting diverse prey fields as they respond to dynamic environments. We reconstructed the historical resource use of albacore tuna (Thunnus alalunga) globally from the 1900s to 2015 and confirmed highly biodiverse diets with 308 prey species, and an additional 238 taxa at coarser taxonomic resolution. We synthesised prey diversity into seven functional trait guilds using hierarchical divisive clustering algorithms as a function of four traits that describe habitat use and influence predator–prey encounter rates – prey habitat association vertically in the water column, horizontally along the coastal to pelagic gradient, seasonal and diel vertical migratory behaviour. We explored variability in historical composition of albacore diets across geographies based on species identity, individual trait information and functional trait guilds using a multi‐matrix modelling framework. Taxonomic information remains important for trophic ecology, however, species‐based diet composition in albacore tuna was highly variable across geographies and years sampled, making interpretation of these patterns difficult. By simplifying species identity into habitat‐based traits, we highlight changes in prey resources consumed, such as the historical importance of near‐surface epipelagic prey resources from coastal to oceanic habitats, and seasonally migrating continental shelf prey, with less frequent pulses of deeper water and demersal taxa. Trait information and trait guilds serve as useful classification frameworks for identifying functionally redundant food web linkages across biodiverse prey, and will prove useful in tracking predators' foraging responses to changing resource availability.