The relative influence of geography, oceanography and environment on gene flow within sessile marine species remains an open question. Detecting subtle genetic differentiation at small scales relevant to marine protected areas is challenging in benthic populations due to large effective population sizes, general lack of resolution in genetic markers, potential microbial associations, and because barriers to dispersal often remain elusive. We genotyped the sponge species Suberites diversicolor using double digest restriction-site associated DNA sequencing (4,826 Single Nucleotide Polymorphisms, SNPs), compared it to same individuals using single markers (COI and ITS), and used previously published data on the associated microbial communities from a subset of the same locations. Studying S. diversicolor from marine lakes at different spatial scales (1-1,400 km), along a gradient of connection to the surrounding sea, and with different environmental regimes, we did not detect strong effects of geographic distance, permeability of seascape barriers or local environments in shaping population genetic structure. All markers detected two major lineages and geographic clustering over a large spatial scale. However, with the SNP dataset we provide new evidence of strong population structure even at scales <10km (average FST = 0.56), where previously none was detected. A lack of congruence between host population structure and microbial community patterns of S. diversicolor from the same locations was observed, suggesting they are on different eco-evolutionary tracks. Our results call for a reassessment of poorly dispersing benthic organisms that were previously assumed to be highly connected based on low resolution markers.