Differences in dispersal among interacting species can generate mismatched population structure and influence the stability of beneficial symbioses. We examined range-wide population genomic structure in the carnivorous pitcher plant Darlingtonia californica and its obligate arthropod associates—the midge Metriocnemus edwardsi and the mite Sarraceniopus darlingtonae—to assess whether these species exhibit shared spatial genetic patterns across the plant’s highly fragmented distribution. We detected broad concordance in population genetic structure among the three species, consistent with shared dispersal pathways across a heterogeneous landscape. In the host plant, genetic diversity declined and genetic differentiation increased toward range margins, patterns that coincided with regions of reduced landscape connectivity.

To investigate the mechanisms underlying these patterns, we quantified landscape connectivity using circuit-theoretic models and compared predicted connectivity with effective migration surfaces inferred from genomic data. Regions of reduced connectivity were associated with lower genetic diversity and reduced effective migration, indicating that spatial constraints on movement contribute to both within- and among-population structure. Landscape genetic analyses revealed contrasting isolation mechanisms across genomes and taxa. Isolation-by-distance was evident in the host’s nuclear genome and in both arthropod symbionts, but was weak in the host’s chloroplast genome, which also exhibited lower overall differentiation than nuclear loci. This pattern suggests that chloroplast variation does not follow a simple distance–decay relationship and may reflect historical or non-equilibrium processes, or alternatively reduced dispersal limitation. In contrast, isolation-by-resistance was detected for the host nuclear genome and for the mite symbiont, indicating sensitivity to landscape structure in these datasets.

Cross-species genetic correlations and cophylogenetic analyses further revealed strong demographic and evolutionary coupling between Darlingtonia and the obligate midge, whereas the mite showed weaker coupling to host population structure but stronger coupling to the midge, consistent with potential codispersal. Together, these results demonstrate how differences in dispersal traits and landscape connectivity jointly shape population genetic structure in this tripartite symbiotic metacommunity.