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Increased temperatures are altering rates of organic matter (OM) breakdown in stream ecosystems with implications for carbon (C) cycling in the face of global change. The metabolic theory of ecology (MTE) provides a framework for predicting temperature effects on OM breakdown, but differences in the temperature dependence of breakdown driven by different organismal groups (i.e., microorganisms vs. invertebrate detritivores) and litter species remain unresolved. Over two years, we conducted 12 60‐day leaf litterbag incubations in 20 headwater streams in the southern Appalachian Mountains (USA). We compared temperature dependence (as activation energy, Ea) between microbial and detritivore‐mediated breakdown, and between a highly recalcitrant (Rhododendron maximum) and a relatively labile (Acer rubrum) leaf species. Detritivore‐mediated breakdown had a higher Ea than microbial breakdown for both leaf species (Rhododendron: 1.48 > 0.56 eV; Acer: 0.97 > 0.29 eV), and Rhododendron breakdown had a higher Ea than Acer breakdown for both organismal groups. Similarly, the Ea of total (coarse‐mesh) Rhododendron breakdown was higher than the Ea of total Acer breakdown (0.89 > 0.52 eV). These effects for total breakdown were large, implying that the number of days to 95% mass loss would decline by 40% for Rhododendron and 26% for Acer between 12°C (our mean temperature value) and 16°C (+4°C, reflecting projected increases in global surface temperature due to climate change). Despite patterns in Ea, overall breakdown rates were higher for microbes than detritivores, and for Acer than Rhododendron over most of our temperature gradient. Additionally, the Ea for a subset of the microbial breakdown data declined from 0.40 to 0.22 eV when fungal biomass was included as a model predictor, highlighting the key role of fungi in determining the temperature dependence of litter breakdown. Our results imply that, as streams warm, routing of leaf litter C to detritivore‐mediated fates will increase faster than predicted by previous studies and MTE, especially for labile litter. As temperatures rise, earlier depletion of autumn‐shed, labile leaf litter combined with rapid breakdown rates of recalcitrant litter could exacerbate seasonal resource limitation and alter carbon storage and transport dynamics in temperate headwater stream networks. [ABSTRACT FROM AUTHOR]