The polychaete Oxydromus okupa lives in association with the bivalves Scrobicularia plana and Macomopsis pellucida in the intertidal of Río San Pedro (CI = Cádiz Intertidal) and adjacent to CHipiona (CH) harbour, and in the subtidal of the Bay of Cádiz (CS = Cádiz Subtidal). We analyse these populations morphometrically, ecologically (including infestation characteristics) and genetically (intertidal populations, 16S and ITS-1 genes). We consider “host”, “environment” and the combined “host and environment” as possible factors of interpopulation variability. Morphometry revealed three well-defined clusters for CI, CH and CS, showing intergroup phenotypic differences ranging from 35 to 50%. Hosts shell lengths ranged between 26 and 36 mm for S. plana and 20 and 28 mm for M. pellucida. The infestation of small M. pellucida by juvenile O. okupa suggests they show an active size segregation behaviour. The intertidal seems to be less favourable (infestation rate <25% vs. up to 65% in the subtidal), and did not show recent bottleneck events. Overall, CI and CH were genetically homogeneous, but showed a significant divergence (one dominant haplotype in each host species), suggesting host shift as being a soft barrier to gene flow. Most characters related with host-entering varied among populations, suggesting symbiotic behaviour to play a key role in reducing panmixia and leading to the initial phases of a speciation process in sympatric symbiotic populations. Polyxeny and symbiotic behaviour in O. okupa seem thus to be underlying mechanisms contributing to its great phenotypic variety, marked ecological differences, and genetic divergence.