Cylindrospermopsis is a cyanobacterial species of global concern, due to its ability to produce potent toxins and its near-cosmopolitan distribution. To date, both management and research efforts for Cylindrospermopsis have focused on riverine settings. By contrast, off-stream storages are inadequately studied, particularly in terms of population dynamics and toxin profiles, how these are linked with the riverine systems that seed them, and what management options are best for optimizing water quality. This is a critical gap, given that storages are key off-take points for many water users, including for livestock watering and industrial supply. This study examined the relationship between a riverine and an off-stream environment, with respect to the development of toxic Cylindrospermopsis blooms in central Queensland. It discusses the role of an aeration system in preventing or delaying bloom development and explores the implications of intake depth with respect to population (cell density) and toxicity. Along the impounded river, the study sites featured warm, stratified conditions and an anoxic hypolimnion. By contrast, the off-stream storage dam lacked stratification, due to the constant aeration provided by a hypolimnetic bubbler. Cylindrospermopsis raciborskii blooms appeared in both environments, with peak cellular concentrations detected in the subsurface waters. The dynamics of the toxin profiles differed, however, with the riverine concentrations being mostly epilimnetic, whereas the dam featured toxin distributed throughout the water column. Concentrations of both cylindrospermopsin (CYN) and deoxy-cylindrospermopsin (deoxy-CYN) were lower in the dam, compared with the riverine sites. A one-month lag period was evident before C. raciborskii cells appeared in the dam following their observation in the river samples, and a similar period elapsed before the dam populations reached their peak concentrations. These data are invaluable in considering the best management options for off-stream sites that experience seeding from riverine populations, particularly for toxin producers such as Cylindrospermopsis.