Bluegill sunfish are one of the classic systems for studying male alternative reproductive tactics (ARTs) in teleost fishes. In this species, there are two distinct life histories: parental and cuckolder, encompassing three reproductive tactics, parental, satellite, and sneaker. The parental tactic is fixed, whereas individuals who enter the cuckolder life history transition from the sneaker to the satellite tactic as they grow. For this study, we used RNAseq to characterize the brain transcriptome of the three male tactics during spawning to identify gene categories associated with each tactic and identify potential candidate genes influencing their different spawning behaviors. We found that sneaker males had higher levels of gene differentiation compared to the other two tactics, suggesting that life history does not exclusively drive differential gene expression. Sneaker males had high expression in ionotropic glutamate receptor genes, specifically AMPA receptors, which may be important for increased working spatial memory while attempting to cuckold nests in bluegill colonies. We also found significant expression differences in several candidate genes involved in ARTs that were previously identified in other species and suggest a previously undescribed role for cytosolic 5-nucleotidase II (nt5c2) in influencing parental male behavior during spawning.