Many harmful cyanobacterial genera have strains that can produce potent toxins and other biologically active compounds that present a risk to the health of humans and other animals that consume or contact contaminated water. Cylindrospermopsins (CYNs) are produced by several species of cyanobacteria including Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju. Previous studies have used filtration methods to separate between the particulate and dissolved CYNs pools. Filtration may lyse cells and thus overestimate the dissolved CYNs pool. Here we employed a novel passive sampling technique to measure the proportion of dissolved CYNs in two Australian strains of C. raciborskii over the growth cycle while minimizing potential overestimation of the dissolved CYNs pool. We simultaneously compared the ratios of the two major CYNs produced by Australian strains of C. raciborskii: cylindrospermopsin (CYN) and deoxy-CYN in the particulate and dissolved pools. CYNs stayed within the cells during log phase but accumulated in the water column during stationary and senescent phases. The proportion of deoxy-CYN to CYN differed between strains but increased in both as cells aged. We conclude that while active release or leaking of CYNs from actively growing cells does occur, CYNs in the water column were primarily a result of cell lysis during stationary phase or due to other environmental stressors. The production of CYN and deoxy-CYN were a constitutive process and both the concentration of, ratio between, and release of CYN and deoxy-CYN were strain dependent. Future studies must account for the genetic diversity of CYN producers when investigating the production of CYNs in natural systems.