Although population genomics approaches have been successful in identifying regions of the genome shaped by natural selection, the progress in dissecting the molecular mechanisms of adaptive variants and traits has been slow. By integrating multi-tissue (gill, spleen, olfactory rosette, whole eye and liver) transcriptomes from 16 wild Eurasian perch (Perca fluviatilis) populations and previously identified footprints of selection based on whole genome scan, we prioritize tissues, candidate genes and putative SNP-gene expression associations involved in humic adaptation of this keystone freshwater fish. Over 5,000 differentially expressed genes (DEGs) were discovered across the five tissues. A significant excess of outlier SNPs among DEGs found in the gill and spleen tissues indicated their involvement in humic adaptation. Further, 3,617 cis-eQTLs that associate with gene expression variation in perch were identified, with approximately 9% of genes harbouring cis-eQTLs showing differential expression between humic and clear-water habitats. Several cis-eQTLs were found in the regions showing most consistent signals of selection also harbouring DEGs (chr. 5: PLAGL2, chr. 7: PPP1R8, TCHH, chr. 8: IFITM3). Thus, our integrative analyses enabled to pinpoint specific organs that play a key role in adaptation, prioritize candidate genes under divergent selection based on their expression patterns, and identify links between SNPs and transcript abundance variation. We expect that the multi-omics strategy outlined in this work provides a practical framework for understanding the genetic basis of phenotypic diversification and adaptation for wide range of species.