Research on the ecological impacts of environmental change has primarily focused at the species level, leaving the responses of ecosystem-level properties like energy flow poorly understood. This is especially so over millennial timescales inaccessible to direct observation. Here we examine how energy flow within a Great Basin small mammal community responded to climate-driven environmental change during the past 12,800 y, and use this baseline to evaluate responses observed during the past century. Our analyses reveal marked stability in energy flow during rapid climatic warming at the terminal Pleistocene despite dramatic turnover in the distribution of mammalian body sizes and habitat-associated functional groups. Functional group turnover was strongly correlated with climate-driven changes in regional vegetation, with climate and vegetation change preceding energetic shifts in the small mammal community. In contrast, the past century has witnessed a substantial reduction in energy flow caused by an increase in energetic dominance of small-bodied species with an affinity for closed grass habitats. This suggests that modern changes in land cover caused by anthropogenic activities--particularly the spread of nonnative annual grasslands--has led to a breakdown in the compensatory dynamics of energy flow. Human activities are thus modifying the small mammal community in ways that differ from climate-driven expectations, resulting in an energetically novel ecosystem. Our study illustrates the need to integrate across ecological and temporal scales to provide robust insights for long-term conservation and management.