Life history theory predicts that parents will balance benefits from investment in current offspring against benefits from future reproductive investments. Long-lived organisms are therefore less likely to increase parental effort when environmental conditions deteriorate. To investigate the effect of decreased foraging capacity on parental behaviour of long-lived monogamous seabirds, we experimentally increased energy costs for chick-rearing thick-billed murres (Uria lomvia). Handicapped birds had lighter chicks and lower provisioning rates, supporting the prediction that long-lived animals would pass some of the costs of impaired foraging ability on to their offspring. Nonetheless, handicapped birds spent less time underwater, had longer inter-dive surface intervals, had lower body mass, showed lower resighting probabilities in subsequent years and consumed fewer risky prey items. Corticosterone levels were similar between control and handicapped birds. Apparently, adults shared some of the costs of impaired foraging, but those costs were not measurable in all metrics. Handicapped males had higher plasma neutral lipid concentrations (higher energy mobilisation) and their chicks exhibited lower growth rates than handicapped females, suggesting different sex-specific investment strategies. Unlike other studies of auks, partners did not compensate for handicapping, despite good foraging conditions for unhandicapped birds. In conclusion, parental murres and their offspring shared the costs of experimentally increased foraging constraints, with females investing more than males.