piRNAs are key regulators of transposable elements (TEs) that have been also shown to have strong effects on gene expression. Since piRNAs are transmitted maternally, they play a key role in maintenance of genome defense across generations. The degree to which they contribute to variation in gene expression across generations is poorly known. Here, using a syndrome of hybrid dysgenesis in D. virilis, we evaluate how gene expression profiles differ in progeny whose mothers greatly differ in their piRNA profile. Moreover, because gonadal atrophy occurs in about 50% of progeny of the dysgenic cross, we can contrast the maternal effects of a divergent piRNA pool with the effects on gene expression that arise from loss of the germline. We have evaluated these contrasting effects by performing RNA-seq on head and thorax tissue of reciprocal males and females, with and without atrophied gonads. We find that differences in maternal piRNA contribution have little to no effect on gene expression in the heads and thorax of progeny. However, when we compare expression profiles of flies with ovaries to genetically identical flies that lack ovaries, but share the same maternal piRNA profile, we find that germline ablation results in changes in the expression of metabolic and neuronal genes in tissues distant from the germline. This indicates that the effects of germline ablation contribute more strongly to somatic gene expression than the maternal effects of piRNA. Interestingly, we do not find significant differential gene expression of genetically and epigenetically identical males with and without testes. This indicates that maintenance of male sex organs in D. virilis has little consequence on gene expression of somatic tissues outside of the abdomen.