Astrangia poculata is a temperate scleractinian coral that exists in facultative symbiosis with the dinoflagellate alga Breviolum psygmophilum across a range spanning the Gulf of Mexico to Cape Cod, Massachusetts. Our previous work on metabolic thermal performance of Virginia (VA) and Rhode Island (RI) populations of A. poculata revealed physiological signatures of cold (RI) and warm (VA) adaptation of these populations to their respective local thermal environments. Here, we used whole-transcriptome sequencing (mRNASeq) to evaluate genetic differences and identify potential loci involved in the adaptive signature of VA and RI populations. This dataset includes sequencing data from 40 A. poculata individuals, including 10 colonies from each population and symbiotic state (VA-white, VA-brown, RI-white, and RI-brown). Our results indicate that differentiation of VA and RI populations in the coral host was driven by putatively adaptive loci, not neutral divergence. In contrast, we found evidence of neutral population differentiation in B. psygmophilum. The opposing pattern of neutral differentiation in B. psygmophilum, but not the A. poculata host, reflects the contrasting dynamics of coral host and algal symbiont population connectivity, dispersal, and gene by environment interactions.