Passion fruit (Passiflora edulis) production is significantly limited by sporadic cold stress events in unfavorable years. The existence of cultivars with varying cold tolerance offers opportunities for genetic improvement of this high-value crop. To elucidate the molecular basis of cold adaption in passion fruit, we conducted an integrated transcriptomic and metabolomic analysis comparing cold-tolerant and cold-sensitive passion fruit cultivars under low-temperature stress. Our multi-omics approach revealed that cold tolerance is associated with significant reprogramming of key pathways, particularly sphingolipid metabolism, phenylpropanoid metabolism, and terpene metabolism. We further validated that exogenous application of the key metabolites within these pathways, sphinganine, chlorogenic acid (CGA), rutin, and three terpenoids enhanced cold tolerance in cold-sensitive cultivars. Conversely, virus-induced gene silencing (VIGS) of core biosynthetic genes (e.g. PesSPT, PesKDSR, PesHCT, and PesFG2) in these pathways compromised cold resistance, leading to increased oxidative damage and more severe phenotypic injury. This study provides comprehensive insights into the molecular networks underlying cold tolerance in passion fruit, highlighting potential candidate genes and metabolites. Our findings establish a crucial foundation for future molecular breeding strategies aimed at improving cold resistance in this profitable horticultural crop.

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