Bull trout (Salvelinus confluentus) research has historically focused on highly impacted systems or occurred in a reactionary manner following overharvest. Here, we used telemetry and multi‐state capture–recapture modelling to inform management decision‐making for this highly migratory, conservation‐listed species in British Columbia's upper Fraser River watershed (UFW). Our work reduced critical information gaps surrounding the seasonal migration patterns, distribution, and survival rates of fluvial bull trout within the region. By using results of an existing microsatellite DNA analysis, we were able to assign each tagged individual to one of five spawning populations. This assignment allowed us to investigate potential differences in migratory behaviour and seasonal habitat use among the different spawning populations. We identified that the majority of tagged UFW fluvial bull trout made repeated, long‐distance migrations (>300 km one direction) to appropriate spawning, overwintering and foraging habitats. The five populations did not vary in their seasonal transition probabilities at the spatial scale investigated, suggesting key habitats are important to multiple populations. We also detected post‐spawning migration and distribution patterns that suggest UFW bull trout exploit seasonal resource pulses during salmon smolt outmigration. Our results highlight the importance of protecting, restoring and maintaining a diverse assemblage of complex habitats and the natural connections between them (e.g. between tributary spawning habitats and larger rivers) at a spatial scale that supports migratory bull trout life histories. This work provides valuable information for prioritizing conservation actions and identifying restoration opportunities both in the UFW and across the species' range.