Controlling foodborne diseases requires robust outbreak detection and a comprehensive understanding of outbreak dynamics. Here, by integrating large-scale phylogenomic analysis of 3,642 isolates and epidemiological data, we performed ‘data-driven’ outbreak detection and described the long-term outbreak dynamics of the leading seafood-associated pathogen, Vibrio parahaemolyticus, in Shenzhen, China, over a 17-year period. Contradictory to the widely accepted notion that sporadic patients and independent point-source outbreaks dominated foodborne infections, we found that 71% of isolates from patients grouped into within-1-month clusters that differed by ≤6 single nucleotide polymorphisms, indicating putative outbreaks. Furthermore, we showed that despite the long time spans between clusters, 70% of them were genomically closely related and were inferred to arise from a small number of common sources, which provides evidence that hidden persistent reservoirs generated most of the outbreaks rather than independent point-sources. Phylogeographical analysis further revealed the geographical heterogeneity of outbreaks and identified a coastal district as the potential hotspot of outbreaks and as the hub and major source of cross-district spread events. Our findings provide a comprehensive picture of the long-term spatiotemporal dynamics of foodborne outbreaks and present a different perspective on the major source of foodborne infections, which will inform the design of future disease control strategies.