The evolution of heteromorphic sex chromosomes has repeatedly resulted in sex chromosome-specific forms of regulation, however how the X chromosome is regulated in the Drosophila male germline has been unclear. In Drosophila melanogaster expression of transgenes driven by spermatogenesis-specific promoters show significantly lower expression on the X chromosome compared to the autosomes. The ~3-fold or greater difference in X-autosome expression is established premeiotically, suggesting that this regulatory process is distinct from canonical sex chromosome dosage compensation or meiotic sex chromosome inactivation. We use transgenes and chromosomal transpositions to compare X and autosomal expression across multiple tissues and find that both non-specific and testis-specific endogenous X-linked genes are transcriptionally suppressed ~2-4-fold specifically in male germline cells. However, in wildtype testes, this sex-chromosome transcriptional suppression is undetectable, as it is effectively compensated by the evolution of strong promoters at X-linked genes. We identify one promoter element sequence motif, in particular, that is enriched immediately upstream of transcription start sites of testis-specific genes, evolutionary conserved across species, associated with increased expression in the testes, and overrepresented on the X. We transgenically validate that this promoter element and show via site-directed mutagenesis that it results in 2-4-fold increased expression in the testes, effectively offsetting X suppression.. Our results help clarify how the X chromosome is regulated in the Drosophila male germline and show that global expression of X-linked genes reflects a balance between chromosome-wide epigenetic transcriptional suppression and long-term compensatory evolution. Our results have broad implications for the evolution of gene expression in the Drosophila male germline and for genome evolution.