Wildlife populations are being increasingly challenged by a variety of anthropogenic stressors including climate change, introduction of non-native species, and encroachment of domestic livestock, which can favor parasite infestation and invasive parasites. For instance, the pathogenic strongyle Haemonchus contortus proliferated in Alberta, Canada, during the last decade. Parasites negatively impact host fitness through a variety of mechanisms ranging from diversion of resources, damage to tissues, and costly immune responses, with consequent impacts on population health and dynamics, in both domestic and wild animals. Therefore, determining and monitoring parasite abundance and community is of primary importance for pathogen control strategies and long-term management of populations. We aimed in this study to update and refine our knowledge on gastrointestinal and protostrongylid nematode parasite communities of bighorn sheep populations from western Canada. Using fecal samples collected from 13 herds of free-living bighorn sheep, mostly from across the province of Alberta, (1) we performed parasitological analyses to morphologically assess the diversity and abundance of gastrointestinal and respiratory strongyles using Wisconsin and Baermann techniques, respectively, and (2) we applied the non-invasive metabarcoding approach to precisely determine gastrointestinal nematodes communities (termed the “nemabiome”). Nematodirus spp. and Marshallagia marshalli were found in greater than 94% of the populations, while strongyles in 65%, with high variations of infestation intensity. Deep-sequencing revealed different species of Nematodirus (N. andersoni, N. davtiani, N. oiratianus) and of gastro-intestinal strongyles, including species shared with domestic ungulates (e.g., Oesophagostomum venulosum, Teladorsagia circumcincta, Ostertagia ostertagi). Moreover, lungworms were isolated in all populations wherein it was discovered that Protostrongylus spp. was the predominant genus present. Our results revealed heterogeneity of parasite abundance and diversity among populations of bighorn sheep in southwestern Canada, and suggest cross-contamination with domestic ungulates.