The apple snail, Pomacea canaliculata (Lamarck, 1819), a freshwater snail listed as a pernicious invasive alien species by the World Conservation Union (IUCN), has caused serious agricultural and ecological harm worldwide. This species has inflicted significant agricultural and ecological damage on a global scale. Under conditions of extreme environmental stress, the apple snail enters a state of dormancy and remains in this dormant phase until environmental conditions become favorable again, which serves as a crucial survival strategy. In our study, we subjected apple snails to 30 days of air-exposure stress followed by rehydration to reactivate them. Our objective was to elucidate the underlying mechanisms associated with drought tolerance, dormancy, and subsequent arousal based on transcriptomic analyses. The results indicated that the groups subjected to 5-, 15- and 30-day air-exposure stress treatments (DRY05, DRY15 and DRY30) exhibited a general down-regulation of metabolism-related pathways. These pathways included starch and sucrose metabolism, linoleic acid metabolism, glutathione metabolism and glycosaminoglycan degradation, compared with the control (CK). In addition, the weighted correlation network analysis (WGCNA) identified two critical pathways: toll-like receptor signaling pathway and adherens junction. The down-regulation of these pathways indicated a decrease in immune levels during dormancy in apple snails. This may further lead to the inhibition of apoptosis and a reduction in energy expenditure, thereby sustaining vital activities. The up-regulation of intercellular adhesion and immune-related pathways upon reawakening (RCY01) further substantiates the presence of this tolerance mechanism during dormancy in the apple snail. This study provides a reference for understanding the tolerance of apple snails to extreme environments, and provides a basic theory for apple snail biocontrol research.