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In marine species, the transcriptomic response to Deepwater Horizon (DWH) oil implicated many biochemical pathways, with corresponding adverse outcomes on organ development and physiological performance. Terrestrial organisms differ in their mechanisms of exposure to polycyclic aromatic hydrocarbons (PAHs) and their physiological challenges, and may reveal either distinct effects of oil on biochemical pathways or the generality of the responses to oil shown in marine species. Using a cross-species hybridization microarray approach, we investigated the transcriptomic response in the liver of Seaside Sparrows (Ammospiza maritima) exposed to DWH oil compared with birds from a control site. Our analysis identified 295 genes differentially expressed between birds exposed to oil and controls. Gene ontology (GO) and canonical pathway analysis suggested that the identified genes were involved in a coordinated response that promoted hepatocellular proliferation and liver regeneration while inhibiting apoptosis, necrosis, and liver steatosis. Exposure to oil also altered the expression of genes regulating energy homeostasis, including carbohydrate metabolism and gluconeogenesis, and the biosynthesis, transport and metabolism of lipids. These results provide a molecular mechanism for the long-standing observation of hepatic hypertrophy and altered lipid biosynthesis and transport in birds exposed to crude oil. Several of the activated pathways and pathological outcomes shown here overlap with the ones altered in fish species upon exposure to oil. Overall, our study shows that the path of oil contamination from the marine system into salt marshes can lead to similar responses in terrestrial birds to those described in marine organisms, suggesting similar adverse outcomes and shared machinery for detoxification.