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Abstract Deepwater Horizon oil spill, the foundation plant speciesSpartina alterniflora proved resilient to heavy oiling, providing an opportunity to identify mechanisms of response to the anthropogenic stress of crude oil exposure. We assessed plants from oil‐affected and unaffected populations using a custom DNA microarray to identify genomewide transcription patterns and gene expression networks that respond to crude oil exposure. In addition, we used T‐DNA insertion lines of the model grassBrachypodium distachyon to assess the contribution of four novel candidate genes to crude oil response. Responses inS. alterniflora to hydrocarbon exposure across the transcriptome as well as xenobiotic specific response pathways had little overlap with those previously identified in the model plantArabidopsis thaliana . Among T‐DNA insertion lines ofB. distachyon , we found additional support for two candidate genes, one (ATTPS21) involved in volatile production, and the other (SUVH5) involved in epigenetic regulation of gene expression, that may be important in the response to crude oil. The architecture of crude oil response inS. alterniflora is unique from that of the model speciesA. thaliana, suggesting that xenobiotic response may be highly variable across plant species. In addition, further investigations of regulatory networks may benefit from more information about epigenetic response pathways.