Freshwater blooms of the microcystin-producing (toxigenic) cyanobacterium Microcystis may cause severe damage to human health and the environment. However, toxigenic and non-toxigenic strains co-exist within single blooms, and microcystin concentration in the water varies throughout the season. We hypothesized that strains that produce and do not produce microcystins represent different genotypes. To this end, we combined microcystin analysis with genomic analyses of individual strains isolated from a natural bloom of the morphospecies Microcystis botrys. Whole-genome assemblies revealed high genomic diversity among 19 strains, representing five different genospecies. Ten strains had intact microcystin cluster with all ten genes (mcyA-J) present and the nine remaining strains lacked all mcy genes. All non-microcystin producing strains were members of a single genospecies, while the microcystin producers were distributed across four different genospecies. One strain had all ten genes present but detectable levels of microcystin were not measured, possibly due to phenotypic plasticity in gene expression or genetic inactivation. Overall, these results demonstrate that even single-morphospecies blooms, from a single time point, consist of multiple populations of genospecies, with different microcystin genotypes and phenotypes. These findings are of great value to the field as the two common observations, presence of toxigenic and non-toxigenic strains within a single bloom and seasonal succession of toxigenicity, can now be attributed to species co-existence and species succession.