Mosquitoes are a disease vector with a complex ecology involving interactions between transmissible pathogens, endogenous microbiota, and human and animal blood meal sources. Unbiased metatranscriptomic sequencing of individual mosquitoes offers a straightforward and rapid way to characterize these dynamics. Here, we profile 148 diverse wild-caught mosquitoes collected in California, detecting sequences from eukaryotes, prokaryotes, and over 70 known and novel viral species. Because we sequenced singletons, it was possible to compute the prevalence of each microbe and recognize a high frequency of viral co-infection. By analyzing the pattern of co-occurrence of sequences across samples, we associated “dark matter” sequences with recognizable viral polymerases and animal pathogens with specific blood meal sources. We were also able to detect frequent genetic reassortment events in a highly prevalent quaranjavirus undergoing a recent intercontinental sweep. In the context of an emerging disease, where knowledge about vectors, pathogens, and reservoirs is lacking, the approaches described here can provide actionable information for public health surveillance and intervention decisions.