The population of Amur ide (Leuciscus waleckii) in Lake Dali, Inner Mongolia, China, has rapidly evolved from a freshwater to an alkali-adapted species within a span of less than 10,000 years, adapting to the challenges posed by high alkalinity and pH levels in closed lake environments. Throughout this transition, the Amur ide in Lake Dali has developed diverse mechanisms of phenotypic plasticity, enabling bidirectional transitions between alkali and freshwater habitats within a single generation. However, the genetic basis underlying this phenotypic plasticity remains incompletely understood. To address this gap, we initially compared genomes of Amur ide individuals from alkali-adapted and freshwater populations, revealing a significant reduction in genetic diversity within the alkali-adapted population and identifying a limited number of sites under positive selection through selection sweeps. This asymmetric relationship between genetic diversity and phenotypic plasticity led us to hypothesize that small, isolated populations of Amur ide in alkali-adapted waters may rely on epigenetic and genetic variations to facilitate phenotypic plasticity. To explore this hypothesis, we investigated the role of DNA methylation in the adaptation of alkali-adapted populations to extreme environments. Using indoor simulations of alkaline stress and freshwater recovery, we examined dynamic changes in DNA methylation and gene transcription in gill tissues. Our results indicate that alterations in gene expression related to immune response, osmotic regulation, and hypoxia induction under alkali-adapted stress are closely associated with dynamic regulation of DNA methylation. Importantly, comparison of adaptive epigenetic variation sites with genetic sites revealed distinct mechanisms of adaptation primarily driven by genetic and epigenetic variations, emphasizing independent roles for epigenetic variation in adaptation. In summary, our study offers novel insights into the molecular mechanisms of phenotypic plasticity, which are critical for predicting adaptive potential in aquatic species facing rapid environmental changes.