Headwater streams are predicted to warm with climate change, altering the microbial processes that control leaf litter decomposition. In this study, we integrate Dakota concepts of Očhéthi (origin/home camp, representing genetic inheritance) and Wóuŋspe (learning through lived experience, representing phenotypic plasticity) to examine how tree origin and growth history shape microbial responses to stream warming. We asked: How do the genetic origin, Očhéthi, and growth environment, Wóuŋspe, of Fremont cottonwood (Populus fremontii) influence microbial growth and leaf litter decomposition under simulated stream warming? We used cuttings from two genetically distinct provenances (warm and cold adapted) and grew them for five years in two common gardens (hot and cold), creating four leaf types. Leaves were then decomposed for 35 days in 48 flow-through stream mesocosms across three temperature treatments (ambient, +3°C, +6°C). We measured decomposition via mass loss and quantified taxon-specific microbial growth rates for fungi and bacteria using quantitative stable isotope probing (qSIP) and DNA sequencing. Tree population, Očhéthi, was the strongest predictor of microbial growth rates and litter mass loss, while a significant population × garden interaction showed that genetic effects depended on climate of growth, Wóuŋspe. This study bridges tree Očhéthi and Wóuŋspe with microbial processes, highlighting the connected roles of plants, microbes, and temperature in influencing litter decomposition and the stability of headwater streams in a warming climate.