Climate change poses a significant threat to biodiversity, highlighting the urgent need to understand species' adaptive potential. Using the sky island limestone-endemic shrub Lonicera oblata in North China as a model, we integrated genomic, transcriptomic, and metabolomic analyses to investigate its evolutionary trajectory. The assembled genome is 786.92 Mb in size, and it has the highest proportion of repetitive sequences (66.47%) in Lonicera. Multiple expanded gene families were enriched in pathways related to stress response, including oxidoreductase activity, cell wall synthesis, and energy metabolism. The bHLH gene family exhibits both a significant expansion in the comparative genomic analysis and a convergent transcriptional activation under calcium stress, correlating with the metabolic reprogramming of organic acid synthesis and ion homeostasis. We detected low genetic diversity (π: 2.24e-3 to 2.80e-3), high differentiation (average fixation index: 0.16), drastic historical decline, and strong genetic load among populations. Notably, the northeasternmost and most recently diverged population (Jiankou) exhibited extreme inbreeding but the lowest genetic load, suggesting that genetic purging enhances small population survival. The genotype-environment association analysis identified 1,286 core SNPs potentially correlated with local adaptation. Genomic offset projections predicted high maladaptation risk under future climates, especially in eastern and southern populations. This study provides essential insights into the mechanisms of local adaptation, genomic vulnerability, and climate resilience of threatened sky island species, and offers guidance for targeted conservation strategies.