The diversification of a host organism can be influenced by both the external environment and its assemblage of microbes. Here, we use a young lineage of spiders, distributed along a chronologically arranged series of volcanic mountains, to determine the evolutionary history of a host and its associated microbial communities, altogether forming the “holobiont”. Using the stick spider Ariamnes waikula (Araneae, Theridiidae) on the island of Hawai’i, and outgroup taxa on older islands, we tested whether the host spiders and their microbial constituents have responded in similar ways to the dynamic abiotic environment of the volcanic archipelago. The expectation was that each component of the holobiont (the spider hosts, intracellular endosymbionts, and gut microbiota) should show a similar pattern of sequential colonization from older to younger volcanoes. In order to investigate this, we generated ddRAD data for the host spiders and 16S rRNA gene amplicon data from their microbiota. Results showed that the host A. waikula is strongly structured by isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different between Ariamnes species on different islands, but more homogenized among A. waikula populations. In contrast, the gut microbiota was largely conserved across all populations and species, and probably mostly environmentally derived. Our results highlight the different evolutionary trajectories of the distinct components of the holobiont, showing the necessity of understanding the interplay between components in order to assess any role of the microbial communities in host diversification.