Upland forest soils are typically major atmospheric carbon dioxide (CO2) sources and methane (CH4) sinks, but the contributions of root and microbial processes, as well as their separate temporal responses to environmental change, remain poorly understood. This 2‐year study was conducted in a temperate, deciduous forest located on the Chesapeake Bay in Maryland, USA. We used temporal CO2 and CH4 flux measurements, exclusion‐source partitioning, and an ecosystem‐scale flooding experiment to understand how carbon (C) fluxes, and their root and microbial sources, respond to seasonal and episodic environmental change. We show that the root‐and‐rhizosphere component of soil CO2 and CH4 flux is significant and that its dependence on soil temperature and volumetric water content (VWC) influences soil C dynamics at seasonal timescales. Experimental flooding shows that CO2 and CH4 flux responses to episodic moisture change were driven by suppression of soil heterotrophs, while root respiration did not respond to transient hydrologic disturbance. Methane uptake responded strongly to episodic inundation, reinforcing the important role of soil moisture in the short‐term control of the forest soil CH4 sink. However, despite the clear seasonality of CH4 uptake, as well as its strong response to short‐term experimental inundation, temperature and VWC were weak predictors of CH4 uptake at a seasonal timescale. We suggest that CH4 consumption in the long‐term may be determined by vegetation, nutrients, microbial communities, or other factors correlated with seasonal changes. Our results indicate that root and microbial sources of both CO2 and CH4 flux respond differently in timing and magnitude to seasonal and episodic environmental change.