The Chlamydomonas monoica Strehlow zygospore is a dormant heavily walled spore adapted to survive extreme environmental conditions. The zygospore wall is multilayered and includes an acetolysis-resistant component related to the general class of compounds referred to as sporopollenin. Germination of the zygospore requires induction and completion of nuclear meiotic divisions, cytokineses to produce the four vegetative progeny cells, and breakdown of the zygospore wall to allow progeny release. Analysis of zygospore wall breakdown by transmission electron microscopy of synchronously germinating zygospores revealed differences in the timing and nature of disintegration of the various wall layers. Breakdown of the outer trilamellar sheath occurred within 6 h after light induction, concomitant with the onset of prophase I. At the same time, stored lipid bodies were consumed and replaced by large cytoplasmic vacuoles. Degradation of the inner more massive wall layer was initiated several hours later at about the time of the second meiotic division. In areas beneath breaks in the trilamellar sheath, a fibrous electron opaque bridge of wall material was retained whereas degradation of the remainder of the inner layer progressed. Finally, disintegration of this bridge material, after the completion of the meiotic divisions and synthesis of progeny cell walls, resulted in the opening of large slits in the trilamellar sheath, allowing escape of the flagellated vegetative progeny. The chloroform resistance typical of mature zygospores was lost at approximately the same time that the initial breaks in the trilamellar sheath were detected but before disintegration of the inner wall layer(s).