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ABSTRACT There is increasing evidence for the co‐occurrence of adaptive within‐generation (WGP) and transgenerational (TGP) plasticity and the ecological scenarios driving both types of plasticity. However, some aspects of their transcriptional mechanisms, such as the role of alternative splicing and the consequences of parental acclimation across life stages, have remained elusive. We explore these fundamental questions by considering the desert endemicDrosophila mojavensisfor which prior evidence indicates adaptive thermal acclimation within and across generations. We implement a full factorial design to estimate genome‐wide patterns of differential gene expression (DE) and alternative splicing (AS) in response to acclimation treatments performed in the parental and offspring generations, as well as considering larval and adult stages. Our results demonstrate that mechanisms of alternative splicing represent a substantial difference between WGP and TGP. These mechanisms contribute substantially to transcriptional plasticity within generations but not across generations. We found a great number of genes associated with transcriptional TGP, which is exclusive to larval stages and not adult samples. Finally, we provide evidence demonstrating opposing transcriptional trajectories in differential gene expression between WGP and TGP. Thus, parental acclimation appears to up‐regulate genes that are down‐regulated during offspring acclimation. This pattern suggests a possible hypothesis for the mechanisms explaining the compensatory effect of parental acclimation in the offspring generation.