Across heterogeneous landscapes, populations may have adaptive differences in gene regulation that adjust their physiologies to match local environments. Such differences could have origins in acclimation or in genetically fixed variation between habitats. Here we use common garden experiments to evaluate differences in gene expression between populations of the purple sea urchin, Strongylocentrotus purpuratus, spanning 1700 km and average temperature differences of 5 °C to 8 °C. Across expression profiles from 18,883 genes after three years of common conditions, we find highly correlated expression patterns (Pearson’s r = 0.992) among most genes. However, sixty-six genes were differentially expressed, including many ribosomal protein and biomineralization genes, all of which had higher expression in urchins originally from the southern population. Gene function analyses revealed slight but pervasive expression differences in genes related to ribosomal function, metabolism, transport, “bone” development, and response to stimuli. In accord with gene expression patterns, a post-hoc spine re-growth experiment revealed that urchins of southern origin re-grew spines at a faster rate than northern urchins. These results suggest that there may be genetically controlled, potentially adaptive differences in gene regulation across habitats and that gene expression differences may be under strong enough selection to overcome high dispersal-mediated gene flow in this marine species.