Despite growing appreciation of the importance of temperature variation, most studies exploring molecular and physiological responses to temperature have focused on constant temperature treatments. To gain a comprehensive understanding of the impacts of fluctuating temperatures, we investigated impacts of increased temperature variation on Phanaeus vindex dung beetles across levels of biological organization. Specifically, we hypothesized that increased temperature variation is energetically demanding, and we predicted that both thermal sensitivity of metabolic rate and energetic reserves would be reduced under increasing amplitudes of fluctuation. To test this hypothesis, we examined metabolic responses of Phanaeus vindex dung beetles exposed to either constant (20°C), low fluctuation (20 ± 5°C), or high fluctuation (20 ± 12°C) temperature treatments using respirometry, energetic reserves, and HPLC-MS-based metabolomics. We found no significant differences in metabolic rates or energetic reserves among treatments, suggesting that the increased fluctuations were not energetically demanding. To understand why there was no effect of increased amplitude on energetics, we assembled and annotated a de novo transcriptome, finding non-overlapping transcriptomic and metabolomic responses of beetles exposed to different amplitudes of temperature variation. Of the 462 metabolites that remained after filtering, we found that 58 metabolites increased in abundance in both fluctuation treatments, but 15 (mostly glycerophospholipids) only did so in response to high amplitude fluctuations. We found 120 transcripts that were significantly upregulated following acclimation to any amplitude of fluctuation, but 274 that were upregulated only in beetles from the low amplitude fluctuation, and 174 that were upregulated only in beetles from the high amplitude fluctuation. Among the differentially expressed transcripts were several associated with post-translational modifications to histones that support a more open chromatin structure. Our results demonstrate that acclimation to different amplitudes of temperature fluctuation is distinct and may be supported by increasing transcriptional plasticity. These data indicate for the first time that histone modifications may underlie rapid acclimation to temperature variation in animals.