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The kuruma shrimp Marsupenaeus japonicas is an economically important crustacean that is widely distributed throughout the Indo-West Pacific. However, M. japonicas exhibits relatively poor thermotolerance properties and frequently suffers from mass mortality during the hot summer months in aquaculture systems. Herein, we performed a comparative transcriptome analysis of M. japonicas in response to heat stress, focusing on immune responses, heat shock proteins, antioxidant systems and metabolism alterations under heat stress. The results revealed that M. japonicas generated adaptive responses to maintain physiological homeostasis under heat stress via the transcriptional up-regulation of heat shock proteins and antioxidant enzymes, enhancement of fatty acid metabolism. However, acute and prolonged exposure to heat stress resulted in the continually decreased expression of immune molecules and led to the repression of glycometabolism, the tricarboxylic acid cycle and the respiratory chain. This study provides a systematic overview of the M. japonicas heat stress response and elucidates potential molecular mechanisms underlying this phenomenon and summer mortality syndrome in this species, which is beneficial for proposing effective strategies to address summer mortality syndrome and promote kuruma shrimp production.