Sewer covers present an interface for biogenic methane (CH4) gas produced in the wastewater collection and transportation system to escape to the atmosphere. However, the contribution of these emissions to municipal CH4 footprints is not well understood. In this study, direct methane emission measurements were made at 118 sewer covers in Calgary, Alberta, Canada to quantify and characterize the emissions from the city's wastewater collection network. Emission rates ranged from 0.00 to 0.241 g CH4 h-1. The annual cumulative wastewater collection emissions are estimated to be 3.92 t CH4 (3.38 to 4.47 t CH4, 95% confidence interval). This is 1.40% of all wastewater treatment-related emissions in Calgary based on a gridded inventory and 0.005% of Calgary's total CH4 footprint according to a city-scale satellite estimate. Sewer covers measured near locations in the wastewater network that are known to be more favorable environments for CH4 production (n = 27) were found more likely to emit CH4 and had statistically higher emission rates compared to the sewer covers that were not (n = 91). Overall, this study indicates that wastewater collection emissions are small for Calgary relative to other biogenic and thermogenic sources in the city; however, this result might not be indicative of the municipal emission patterns from other cities.