The two major surface proteins of procyclic forms in the insect midgut, EP and GPEET procyclin, are transcribed from a polycistronic transcription unit by RNA polymerase I. We identified a long non-coding RNA, termed TblncRNA-23, that is encoded between the two procyclin genes. TblncRNA-23 was localized to the nucleolus and also associated with polysomes. Overexpression of TblncRNA-23 identified EP and GPEET mRNAs as targets, as well as other mRNAs, that changed abundance in the transition from early to late procyclic forms. TblncRNA-23 interacted with its substrates via base-pairing using different domains. Purification of TblncRNA-23-associated proteins by RaPID identified hundreds of proteins, including proteins translated from its target mRNAs, suggesting association with translating ribosomes. Nucleolar TblncRNA-23 associated with multiple pre-rRNA processing factors, and cytoplasmic TblncRNA-23 with RNA binding proteins that regulate mRNA stability and translation. Early and late procyclic forms differ in their social motility (SoMo) capabilities, which is essential for migration away from the insect midgut to enable parasite transmission. Overexpression of TblncRNA-23 resulted in parasites exhibiting hyperSoMo, suggesting a regulatory role in SoMo and the parasite's potential to cycle between hosts