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Lakes are highly heterogenous ecosystems inhabited by a rich microbiome whose genomic diversity remains poorly defined compared to other major biomes. Here, we present a continental-scale study of metagenomes collected across one of the most lake-rich landscapes on Earth. Analysis of 308 Canadian lakes resulted in a metagenome-assembled genome (MAG) catalogue of 1,008 bacterial genomospecies spanning a broad phylogenetic and metabolic diversity. Lake trophic state was a significant determinant of taxonomic and functional turnover of MAG assemblages. We detected a role for resource availability, particularly carbohydrate diversity, in driving biogeographic patterns. Coupling the MAG catalogue with geomatics information on watershed characteristics revealed an influence of soil properties and human land use on MAG assemblages. Agriculture and human population density were particularly influential on MAG functional turnover, signifying a detectable human footprint in lake bacterial communities. Overall, the Canadian lake MAG catalogue greatly expands the freshwater microbial genomic landscape, bringing us closer to an integrative view of bacterial genome diversity across Earth’s biomes.