Tracheliastes polycolpus is an ectoparasitic copepod that recently emerged in western Europe and that infects several freshwater fish species. Its recent successful spread might be due to its fascinating ability to shift to new host populations and/or species. Here, we present the first non-redundant and protein-coding de novo transcriptome assembly for T. polycolpus along with a quality assessment and reliable transcript annotations. This assembly was built from fifteen adult female parasites sampled from three different host species from a single river in southwestern France. Overall, 17,157 non-redundant contigs likely corresponding to protein-coding transcripts were identified, of which 13,093 (i.e., 76%) were successfully annotated. This assembly displayed good representativeness since 65.8% of the raw reads properly aligned back to the assembly. Similarly, 90.5% of the single copies of orthologues conserved across arthropods were retrieved in this assembly, which reflects a very good completeness. Finally, this transcriptome assembly gathered 7979 T. polycolpus specific transcripts when compared with the two closest referenced species (Lepeophtheirus salmonis and Caligus rogercresseyi), thus constituting an original genomic resource. This high-quality transcriptome is an important genomic resource for deciphering the molecular bases underlying host shifts in generalist parasites, and for studying the evolutionary biology of copepods that are major biological components of both freshwater and marine ecosystems.