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The sea lamprey is an invasive pest in the Great Lakes. Sex-ratio distortion systems for pests are highly effective once other control measures have reduced abundance, so genetic manipulation of sex ratios is being investigated as a complement to existing sea lamprey control. However, a genetic basis for sex determination in lampreys remains elusive. Environmental sex determination (ESD) has been suggested, but the evidence is equivocal, and no fish species with only ESD is known. Using a two-pronged genomics and transcriptomics approach, we suggest that the germline-specific region (GSR) of the genome, the part jettisoned from somatic cells during embryonic development, holds the key. 1) Using whole genome sequences from fin clips of >200 sea lamprey, we found no sex-specific differences in the somatic genome. 2) However, analyzing RNA-sequence data from gonads sampled across developmental stages, we identified 638 germline-specific genes that are highly expressed only in males, and putative orthologs of some of these genes have known functions in sex determination and differentiation in other vertebrates. We conclude that the GSR plays an important role in testicular differentiation, and we propose a mechanism for how environmental and genetic factors work together to control lamprey sex. [ABSTRACT FROM AUTHOR]