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 life history 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 and females 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 male tactics. Sneaker males also had high expression in ionotropic glutamate receptor genes, specifically AMPA receptors, which may be important for increased working spatial memory while attempting to cuckold parental males at their nests. Larger differences in gene expression also occurred among male tactics than between males and females. We found significant expression differences in several candidate genes that were previously identified in other species with ARTs and suggest a previously undescribed role for cAMP-responsive element modulator (crem) in influencing parental male behaviors during spawning.