Adaptation to different ecological environments can promote speciation. Although numerous examples of such ‘ecological speciation’ now exist, the genomic basis of the process, and the role of gene flow in it, remains less understood. This is, at least in part, because systems that are well characterized in terms of their ecology often lack genomic resources. In this study, we characterize the transcriptome of Timema cristinae stick insects, a system that has been researched intensively in terms of ecological speciation, but for which genomic resources have not been previously developed. Specifically, we obtained >1 million 454 sequencing reads that assembled into 84 937 contigs representing approximately 18 282 unique genes and tens of thousands of potential molecular markers. Second, as an illustration of their utility, we used these genomic resources to assess multilocus genetic divergence within both an ecotype pair and a species pair of Timema stick insects. The results suggest variable levels of genetic divergence and gene flow among taxon pairs and genes and illustrate a first step towards future genomic work in Timema.