Abstract Seasonal migration is a physiologically demanding endeavour that animals prepare for by finding and storing energy. Species and populations vary in their tendencies to migrate and the energetic demands of migration likely determine the degree and type of preparation that different animals undergo. Birds fuel their migratory flight using stored fat. Previous work has suggested that in addition to being energetically dense, certain lipids like polyunsaturated fatty acids (PUFAs) may be particularly efficient fuels that are preferentially mobilized for flight or serve may additional functions, such as modulating membrane fluidity or stimulating gene expression as ligands, during long‐distance migratory flight. Using a series of behavioural and metabolic experiments in a partial transplant aviary setting of Common Blackbirds (Turdus merula) populations that range from being fully migratory to partially migratory to sedentary, we asked how migratory restlessness (Zugunruhe), weight gain and oxidation of stearic acid (18:0), oleic acid (18:1n‐9), linoleic acid (18:2n‐6) and alpha linolenic acid (18:3n‐3; ALA) varied with migratory mode and season. We found no population‐level differences in the timing of Zugunruhe. However, before migration, a greater proportion of individuals from fully migratory populations exhibited weight gain and migratory restlessness, as well as increased oxidation of PUFAs. After Zugunruhe, only individuals from migratory populations showed reduced PUFA oxidation. All populations showed increased oxidation of saturated fat after Zugunruhe. Our results demonstrate that certain migratory traits, like the timing of Zugunruhe are expressed similarly across populations in response to local environmental conditions, while other traits, like lipid oxidation, can vary among populations. Read the free Plain Language Summary for this article on the Journal blog.