Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (<300 km) was observed. Host population structure had a moderate effect on the structure of these microbial communities, regardless of geographic distance. These results support the interplay between geographic, environmental, and host factors as forces determining the community structure of microbiomes associated with C. delitrix. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.