Understanding the genetic, and transcriptomic changes that drive the phenotypic plasticity of fitness traits is a central question in evolutionary biology. In this study, we utilised 152 natural Swedish Arabidopsis thaliana accessions with re-sequenced genomes, transcriptomes, and methylomes and measured flowering times under two temperature conditions (10 °C and 16 °C) to address this question. We revealed that the northern accessions exhibited advanced flowering in response to decreased temperature, whereas the southern accessions delayed their flowering, indicating a divergent flowering response. This contrast in flowering responses was associated with the isothermality of their native ranges, which potentially enables the northern accessions to complete their life cycle more rapidly in years with shorter growth seasons. At the transcriptome level, we observed extensive rewiring of gene co-expression networks, with the expression of 25 core genes being associated with the mean flowering time and its plastic variation. Notably, variations in FLC expression sensitivity between northern and southern accessions were found to be associated with the divergence flowering time response. Further analysis suggests that FLC expression sensitivity is associated with differences in CG, CHG and CHH methylation at the promoter region. Overall, our study revealed the association between transcriptome plasticity and flowering time plasticity among different accessions, providing evidence for its relevance in ecological adaptation. These findings offer deeper insights into the genetics of rapid responses to environmental changes and ecological adaptation.