Diapause, a form of insect dormancy, is thought to facilitate overwintering survival by increasing cold tolerance and decreasing energy drain at high temperatures via metabolic rate suppression. Averting diapause prior to winter is generally assumed to be a lethal phenotype. However, metabolic rate and cold tolerance are plastic – they can change following exposure to different environmental conditions. Here, we tested the hypothesis that cold acclimation can induce a diapause-like phenotype, compensating for the potential costs of averting diapause. We tested this in the apple maggot fly, which exhibits segregating genetic variation for diapause intensity (propensity to avert diapause). This fly overwinters in the soil as a diapause pupa, but can avert diapause (non-diapause) or terminate diapause early (shallow diapause) when reared at warm temperatures. We found that diapause, non-diapause, and shallow diapause pupae were freeze-avoidant and had similar tolerance of extreme low temperatures (cooling to c. -18 °C) following two months acclimation at 4 °C. Metabolic rates were higher in non-diapause and shallow diapause than diapause pupae at warm (25 °C) and cool (4 °C) temperatures. Non-diapause and shallow diapause metabolic rates decreased slowly over time at 4 °C, achieving diapause-like metabolic rates. Despite this metabolic flexibility at low temperatures, non-diapause and shallow diapause pupae did not survive prolonged chilling well. We conclude that energy drain at low (not just high) temperatures can contribute to chilling mortality in insects that avert diapause, and cold acclimation can only partially compensate for costs associated with averting diapause.