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Cowpea aphid-borne mosaic virus (CABMV) and Cowpea severe mosaic virus (CPSMV) threaten cowpea commercial production. This study aimed to analyze Conserved Transcriptional Signatures (CTS) in cowpea's genotypes that are resistant to these viruses. CTS covered up- (UR) or down-regulated (DR) cowpea transcripts in response to CABMV and CPSMV mechanical inoculations. The conservation of cowpea's UR defense response was primarily observed with the one hpi treatments, with decreased CTS representatives as time elapsed. This suggests that cowpea utilizes generic mechanisms during its early interaction with the studied viruses, and subsequently employs more specialized strategies for each viral agent. The potential action of the CTS-UR emphasizes the importance of redox balance, ethylene and jasmonic acid pathways. Additionally, the CTS-UR provides evidence for the involvement of R genes, PR proteins, and PRRs receptors-extensively investigated in combating bacterial and fungal pathogens-in the defense against viral inoculation. AP2-ERF, WRKY, and MYB transcription factors, as well as PIP aquaporins and MAPK cascades, also emerged as significant molecular players. The presented work represents the first study investigating conserved mechanisms in the cowpea defense response to viral inoculations, highlighting relevant processes for initial defense responses.