Group-living animals nimbly respond to social challenges and opportunities by changing hormone profiles, neural activity patterns, and gene expression. How these processes are integrated into context-appropriate changes of behavior is not well understood. In vertebrates, this complex process depends on the distributed activity of a highly interconnected and conserved set of fore- and midbrain regions known as the social decision making network (SDMN). Here, we use the highly social African cichlid fish Astatotilapia burtoni, a model system in social neuroscience, to characterize the neural transcriptomic response to a social opportunity. We provided subordinate males an opportunity to ascend to dominant status for up to 1 week and quantified behavior and physiology at three time points after the onset of social ascension, followed by an analysis of transcriptomic response of three critical SDMN nodes (homologs of the preoptic area, hippocampus, and extended medial amygdala). We first replicate that behavioral and physiological changes that have previously been shown to accompany social ascent. We then find that the three SDMN nodes we investigated have distinct transcriptomic profiles that change in subtle ways as animals ascend in social status. Finally, we uncover genes and gene co-expression modules that are associated with behavioral and physiological measures, suggesting specific molecular pathways that allow ascending males to take advantage of social opportunity. Taken together, our results provide insight into the neuromolecular changes occurring throughout the process of social ascent.