Improving our understanding of energy allocation in reproduction is key for accurately parameterizing bioenergetic models to assess population responses to environmental perturbations and anthropogenic disturbance. We quantified the energetic cost of gestation in humpback whales (Megaptera novaeangliae) using historical whaling records, non-invasive unoccupied aerial system (UAS) photogrammetry and post mortem tissue samples. First, we estimated relative birth size using body length measurements of 678 mother-fetus pairs from historical whaling records and 987 mother-calf pairs measured in situ using UAS-photogrammetry. The total energetic cost of gestation includes fetal growth (FG), heat increment of gestation and placental tissue development. FG was modelled from conception to birth, with fetal volume and mass estimated using the volume-to-length relationship of perinatal calves and published humpback whale tissue composition estimates. Tissue-specific energy content was quantified using post mortem bone, muscle, viscera and blubber samples from a neonatal humpback whale. Placental tissue development was estimated using humpback whale placental tissue and published equations. Relative birth length was found to be 33.75% (95% CI: 32.10-34.61) of maternal length. FG rates and absolute birth size increased with maternal length, with exponential growth in fetal length, volume and mass resulting in minimal energetic costs over the first two quadmesters (0.01-1.08%) before increasing significantly in the final quadmester (98.92%). Gestational heat constituted the greatest energetic cost (90.42-94.95%), followed by fetal (4.58-7.76%) and placental (0.37-1.83%) tissue growth. Our findings highlight the energetic costs endured by capital breeding females preceding parturition, with the most substantial energetic costs of gestation coinciding with migration and fasting. KEY POINTS: We quantified the energetic cost of gestation using body length measurements of mother-fetus pairs from historical whaling records, length estimates of mother-calf pairs measured in situ using aerial photogrammetry and post mortem tissue samples. Fetal growth rates and birth size increased with maternal length, with fetal length, volume and mass increasing exponentially over gestation. Energetic costs over the first two quadmesters were negligible (0.01-1.08%) before increasing significantly in the final quadmester (98.92%). Though larger females incur nearly twice the energetic cost of smaller females, they are likely buffered by greater absolute energy reserves, suggesting smaller females may be less resilient to perturbations in energy balance. We demonstrate the significant energetic costs incurred by pregnant humpback whales, with most of the energetic expenditure occurring over the final 100 days of gestation. Late-pregnant females are, therefore, particularly vulnerable to disruptions in energy balance, given periods of greatest energetic stress coincide with fasting and migration.