Northern peatlands store globally significant amounts of soil carbon that could be released to the atmosphere under drier conditions induced by climate change. We measured forest floor respiration (RFF) at hummocks and hollows in a treed boreal bog in Alberta, Canada and partitioned the flux into aboveground forest floor autotrophic, belowground forest floor autotrophic, belowground tree respiration, and heterotrophic respiration using a series of clipping and trenching experiments. These fluxes were compared to those measured at sites within the same bog where water‐table (WT) was drawn down for 2 and 12 years. Experimental WT drawdown significantly increased RFF with greater increases at hummocks than hollows. Greater RFF was largely driven by increased autotrophic respiration driven by increased growth of trees and shrubs in response to drier conditions; heterotrophic respiration accounted for a declining proportion of RFF with time since drainage. Heterotrophic respiration was increased at hollows, suggesting that soil carbon may be lost from these sites in response to climate change induced drying. Overall, although WT drawdown increased RFF, the substantial contribution of autotrophic respiration to RFF suggests that peat carbon stocks are unlikely to be rapidly destabilized by drying conditions.