Microbial physiological responses to long-term warming are poorly understood. Here we applied metatranscriptomics to investigate how microorganisms react to medium-term (8 years) and long-term (>5 decades) subarctic grassland soil warming of +6 °C. Decades, but not years, of warming induced changes in relative abundances of eukaryotic, prokaryotic, and viral transcripts and reduced functional richness. However, irrespective of the duration of warming, we observed a community-wide upregulation of central (carbon) metabolisms and cell replication in the warmed soils, whereas essential energy metabolism and protein biosynthesis complexes and pathways were downregulated. This coincided with a decrease of microbial biomass and lower soil substrate concentrations (e.g. dissolved organic carbon and phosphorus). We conclude that permanently accelerated reaction rates at higher temperatures facilitate a downregulation of energy metabolism and protein biosynthesis, potentially freeing energy and matter for substrate acquisition and growth. This resource allocation seems to be a common response in microorganisms and allows sustaining high metabolic activities and replication rates even after decades of soil warming.