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Recent studies have uncovered patterns of genomic divergence in marine teleosts where panmixia due to high gene flow has been the general paradigm. These signatures of divergent selection are often impacted by structural variants, acting as "supergenes" facilitating local adaptation. The highly dispersing European plaice (Pleuronectes platessa)—in which putative structural variants (i.e., inversions) have been identified—has successfully colonized the brackish water ecosystem of the Baltic Sea. Thus, the species represents an ideal opportunity to investigate how the interplay of gene flow, structural variants, natural selection, past demographic history, and gene flow impacts on population (sub)structuring in marine systems. Here, we report on the generation of an annotated draft plaice genome assembly in combination with population sequencing data—following the salinity gradient from the Baltic Sea into the North Sea together with samples from Icelandic waters—to illuminate genome‐wide patterns of divergence. Neutral markers pointed at large‐scale panmixia across the European continental shelf associated with high gene flow and a common postglacial colonization history of shelf populations. However, based on genome‐wide outlier loci, we uncovered signatures of population substructuring among the European continental shelf populations, i.e., suggesting signs of ongoing selection. Genome‐wide selection analyses (xp‐EHH) and the identification of genes within genomic regions of recent selective sweeps—overlapping with the outlier loci—suggest that these represent the signs of divergent selection. Our findings provide support for genomic divergence driven by local adaptation in the face of high gene flow and elucidate the relative importance of demographic history versus adaptive divergence in shaping the contemporary population genetic structure of a marine teleost. The role of the putative inversion(s) in the substructuring—and potentially ongoing adaptation—was seemingly not substantial. [ABSTRACT FROM AUTHOR]