Microcystis aeruginosa is a cyanobacterium frequently associated with toxic blooms in eutrophic freshwater systems. Certain strains produce microcystins (MCs), a group of hepatotoxins with significant ecological and public health implications. In this study, we examined the quantitative response of a temperate native M. aeruginosa strain to combinations of temperature (26, 30, and 36 ◦C), light intensity (30, 50, and 70 μmol photons·m−2·s−1), and N:P ratio (10, 100, 150), using a full-factorial experimental design. Growth parameters (μ, lag phase duration, and maximum cell density), chlorophyll-a production, and MC-LR synthesis were modeled using Gompertz, linear, and dynamic approaches. High temperature and irradiance increased the specific growth rate but decreased final biomass, while elevated N:P ratios shortened the lag phase. MC-LR production peaked under low temperature, low irradiance, and low N:P ratio. Although MC-LR synthesis did not correlate positively with growth rate, and the environmental conditions maximizing growth differed from those enhancing toxin production, a population-level coupling between both processes was observed using the Long model. These findings suggest that MC-LR synthesis in M. aeruginosa is not merely a metabolic by-product of growth, but a context-dependent trait with potential adaptive significance.