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ABSTRACT Adaptive introgression involves the acquisition of advantageous genetic variants through hybridisation, which are subsequently favoured by natural selection due to their association with beneficial traits. Here, we analysed speciation patterns of the kleptoparasitic spider,Argyrodes lanyuensis, through genomic analyses and tested for possible genetic evidence of adaptive introgression at the Taiwan–Philippines transition zone. Our study used highly polymorphic SNPs to demonstrate that speciation occurred when the Hualien (on Taiwan Island + Green Island) and Orchid Island + Philippine lineages separated during the early to mid‐Pleistocene. The best colonisation model suggested by approximate Bayesian computation and random forests and biogeographical analyses supported an inference of a bottleneck during speciation, an interpretation reinforced by observation of lowerF_STvalues and reduced genetic diversity of the Orchid Island + Philippines lineage. We also found the highest support for the occurrence of introgression on the youngest island (Green Island) of the Taiwan–Philippines transition zone based on the ABBA‐BABA test. Our study highlights the inference of two noteworthy species (Hualien + Green Island and Orchid Island + Philippines) based on our species delimitation tests, with gene flow between Green Island and Orchid Island that indicates introgression. The potential adaptive alleles in Green Island population, which are under balancing selection, provide initial evidence of possible rare case of adaptive introgression. This could represent an evolutionary response to a newly formed niche (or novel geographical context) lying between the tropical climate of the Philippines and the subtropical climate of Hualien, Taiwan.