Microbial activities in sub-alpine forest soil influence global cycling of the potent greenhouse gas methane. Understanding the dynamics of methane-oxidizing bacterial communities, particularly the roles of potentially active versus total microbial populations, is necessary for reducing uncertainty in global methane budget estimates. However, our understanding of the factors influencing methane cycling in forest soils is limited by our lack of knowledge about the biology of the microbes involved and how these communities are shaped by their environment. Here, we compared the composition and potential activity of microbial communities using 16S rRNA gene amplicon sequencing of total genomic DNA (gDNA) and potentially active complementary DNA (cDNA) from shallow soil in Red Butte Canyon (Salt Lake City, Utah, USA). We compared riparian and upland soils at two time points in the growing season and found distinct differences in both the community composition of the gDNA and cDNA libraries and the potential drivers of these community structures. Aerobic methane-oxidizing bacteria (methanotrophs) were detected in all samples, with cDNA libraries containing a higher average relative abundance and diversity of methanotrophs compared to gDNA libraries. Methane flux at the sample sites did not significantly correlate to the relative abundance (gDNA) or potential activity (cDNA) of methanotrophs. In the cDNA libraries, there were significant positive correlations between the abundance of Methylococcaceae family methanotrophs and several non-methanotrophic methylotrophs previously found to be associated with methane-oxidizing bacterial communities. These findings suggest a complex relationship between methane-cycling bacterial communities and methane flux and highlight the need for further in situ studies to understand the environmental and ecological influences of these microbial consortia. IMPORTANCE Methane-oxidizing bacteria are found in diverse soil and sediment environments and play an important role in mitigating flux of this potent greenhouse gas into the atmosphere. However, it is unclear how these bacteria and their associated communities are structured in the environment and how their activity ultimately influences methane flux. In this work, we examine the composition and structure of methane-oxidizing bacterial communities in sub-alpine forest soil and find soil- and time-specific differences between the stable and potentially active populations. We also find that the potentially active populations of certain methanotrophs and non-methanotrophs are positively correlated. This work provides a step toward refining our understanding of microbially mediated biogeochemical cycles.