Significance The malaria parasite requires the formation of a stage-specific, enigmatic organelle—the crystalloid—for mosquito invasion. Perhaps acting as storage for proteins and lipids, the crystalloid is generated during ookinete formation and dissolved during sporogony in the oocyst. We show here that Plasmodium berghei expresses an S-acyl-transferase DHHC10 that localizes to the crystalloid. Parasites depleted of dhhc10 produce ookinetes that successfully establish oocysts but fail to produce sporozoites; knockout parasites are characterized by the absence of the crystalloid and the mislocalization of a crystalloid-resident protein.