For apicomplexan parasites using an oral-fecal transmission route with significant environmental exposure, the environmental persistence and infectivity of the oocyst has a direct impact on local infection dynamics, including the ability to withstand extended periods without readily available hosts. Herein we quantify the environmental persistence and infectivity of the oocysts of 2 septate gregarine species at controlled temperature and humidity and demonstrate that they can persist over multiple generational time spans. Species of Blabericola generally complete their endogenous life cycles from oocyst to oocyst within 10 days. The median residual environmental oocyst lifetime for Blabericola oocysts in this study is 21–28 days, but a significant number of oocysts of Blabericola migrator persisted and remained infective in the environment for up to 39 days while those of Blabericola cubensis persisted and remained infective for up to 92 days. Although long-lived relative to their own generational time, the oocysts of Blabericola species infecting cockroaches are short-lived relative to gregarines infecting tenebrionid beetles. For these gregarines, oocysts can persist in the environment and remain infective for up to 787 days. Mechanistically, environmental persistence and infectivity are probably energy-limited phenomena related to the amount of stored amylopectin and the basal metabolic rate of quiescent oocysts.