Transcriptome analysis is a powerful tool for unveiling the distribution and magnitude of genetic incompatibilities between hybridizing taxa. The nature of such incompatibilities is closely associated with the evolutionary histories of the parental species and may differ across tissues and between the sexes. In eusocial insects, the presence of castes that experience divergent selection regimes may result in additional distinct patterns of caste-specific hybrid incompatibilities. We analyzed levels of expression of >14,000 genes in two life stages of each caste and sex in the fire ants S. invicta and S. richteri and in their hybrids. We found strong contributions of both developmental stage and caste to gene expression patterns. Hybrid incompatibilities were surprisingly modest: only 32 genes were mis-expressed, indicating low levels of disruption in gene regulation in hybrids. The castes differed in numbers of mis-expressed genes, with males and workers each mis-expressing at least seven times as many genes as queens. Interestingly, homologues of many of the mis-expressed genes have been implicated in behavioral variation in Drosophila melanogaster. General expression profiles of hybrids were more similar to those of S. richteri than S. invicta, presumably because S. richteri trans-regulatory elements tend to be dominant to those of S. invicta and/or because there is an overall bias in the genetic composition of the hybrids towards S. richteri. Altogether, our results suggest that selection acting on each caste may contribute differently to interspecific divergence and speciation in this group of ants.