Cliona delitrix is one of the most abundant and destructive coral-excavating sponges on Caribbean reefs. However, basic aspects of its reproductive biology, which largely determine the species propagation potential, remain unknown. A 2-year study (October 2009 to September 2011) was conducted to determine the reproductive cycle and gametogenesis of a C. delitrix population located in a shallow reef in Florida, USA. Mesohyl tissue collected from randomly chosen and tagged sponge individuals was sampled one to several times a month, and analysed by light and transmission electron microscopy (TEM). Cliona delitrix is oviparous and gonochoric, except for a few simultaneous hermaphroditic individuals. The C. delitrix reproductive cycle in Florida is from April to December, and is triggered by an increase in seawater temperature to 25°C. Oogenesis and spermatogenesis were asynchronous among individuals; with different cohorts of oocytes co-occurring in females, and spermatic cysts in males. Granulose cells acted as nurse cells, contributing to the growth and maturation of both female and male gametes. Spawning of gametes was not always synchronized with full moon phase. Unlike most other oviparous sponges, the reproductive cycle of C. delitrix is versatile and includes multiple spawning events during the summer of each year. This characteristic maximizes sponge propagation on coral reefs during the warmer months of the year, particularly when thermal stress induces coral mortality. This aspect, combined with its success on polluted areas, make C. delitrix a suitable bioindicator of coral reef health.