The transcriptomes of two distinct physiological moments of root dehydration condition were scrutinized in cowpea. The RD25 (first 25 min after root dehydration imposition) physiological data did not indicate significant alterations. For the other treatment, 150 min under root dehydration (RD150), all physiological data indicated that the studied cultivar was under stress. The physiological differences between RD25 and RD150 reverberated in the respective transcriptomes. The sets of in silico differentially expressed isoforms showed specificity for each treatment time. The comparison of T25 | UR [up-regulated transcripts in T25 (RD25 vs. Cont25)] vs. T150 | UR [up-regulated transcripts in T150 (RD150 vs. Cont150)] enriched GO terms (associated with abiotic stresses), despite certain similarities, showed us that they were associated with the respective physiological moments. Concerning gene families, a large portion of those present in the T25 | UR were associated with signaling processes; for T150 | UR, a miscellany of families (from transcription factors to nonenzymatic proteins) was observed. The plotting of transcriptomics data in the KEGG Pathway database indicated a change in the topology of activated metabolic modules in T25 | UR vs. T150 | UR. For the latter, it was observed that most activated modules were associated with specialized metabolism. C2H2 and BPC1 transcription factors (TFs) sites were enriched at T25 | UR and T150 | UR gene promoters, suggesting the importance of these TFs for cowpea response to root dehydration. Our work provides insights into specific molecular actors and pathways, enhancing our global understanding of cowpea stress response.