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Capacity to cope with warming temperatures is a key determining factor of species' persistence under global climate change. Many successful invasive species have heightened thermal tolerance relative to their native counterparts, which may provide competitive advantages for habitat utilization and resource acquisition under warming scenarios, ultimately contributing to radically altered community composition. Enhanced transcriptional plasticity may be an important factor conferring superior abilities to cope with environmental stress, but the molecular mechanisms driving key differences of organismal traits in invasive versus native species are not well known. Although it is predicted that established invaders will evolve canalized phenotypes well‐adapted to new environments, it is not clear whether the same expectations are true for invaders of variable thermal environments or under climate warming scenarios where abilities to cope with fluctuating and increasing temperatures may provide fitness advantages. Here, we compare a highly successful invasive fish and a sympatric endangered native fish living in a dynamic estuarine environment that is projected to warm under climate change. We linked organismal physiological limits with global transcriptional responses at multiple common relative and absolute temperature thresholds and determined that heightened thermal tolerance of invasive Inland Silversides (Menidia beryllina) is associated with transcriptional changes that are greater both in the number of genes and the magnitude of response relative to native Delta Smelt (Hypomesus transpacificus). Modulated genes contributed to the enrichment of biological processes that differed between species and generally increased with temperature. These results are in concordance with the hypothesis that transcriptional plasticity may play a key role in determining population persistence, species interactions, and shaping community assemblages under climate change. Future studies encompassing a wider range of species and taxa are needed to determine whether this is a general pattern found between native and invasive species more broadly.