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Predicting the persistence of species under climate change is an increasingly important objective in ecological research and management. However, biotic and abiotic heterogeneity can drive asynchrony in population responses at small spatial scales, complicating species-level assessments. For widely distributed species consisting of many fragmented populations, such as brook trout (Salvelinus fontinalis), understanding the drivers of asynchrony in population dynamics can improve the predictions of range-wide climate impacts. We analyzed the demographic time series from mark-recapture surveys of 11 natural brook trout populations in eastern Canada over 13 years to examine the extent, drivers, and consequences of fine-scale population variation. The focal populations were genetically differentiated, occupied a small area (~25 km² ) with few human impacts, and experienced similar climate conditions. Recruitment was highly asynchronous, weakly related to climate variables and showed population-specific relationships with other demographic processes, generating diverse population dynamics. In contrast, individual growth was mostly synchronized among populations and driven by a shared positive relationship with stream temperature. Outputs from population-specific models were unrelated to four of the five hypothesized drivers (recruitment, growth, reproductive success, phylogenetic distance), but variation in groundwater inputs strongly influenced stream temperature regimes and stock-recruitment relationships. Finally, population asynchrony generated a portfolio effect that stabilized regional species abundance. Our results demonstrated that population demographics and habitat diversity at microgeographic scales can play a significant role in moderating species responses to climate change. Moreover, we suggest that the absence of human activities within study streams preserved natural habitat variation and contributed to asynchrony in brook trout abundance, while the small study area eased monitoring and increased the likelihood of detecting asynchrony. Therefore, anthropogenic habitat degradation, landscape context, and spatial scale must be considered when developing management strategies to monitor and maintain populations that are diverse, stable, and resilient to climate change.