The most damaging pathogen in blackcurrant plantations is mite-transmitted blackcurrant reversion virus (BRV). Some Ribes species have an encoded genetic resistance to BRV. We performed RNA sequencing analysis of BRV-resistant blackcurrant cv. Aldoniai to evaluate the molecular mechanisms related to the BRV infection response. The RNA of virus-inoculated and mock-inoculated microshoots was sequenced, and the transcriptional changes at 2- and 4-days post inoculation (dpi) were analyzed. The accumulation and expression of BRV RNA1 were detected in infected plants. In total, 159,701 transcripts were obtained and 30.7% were unigenes, annotated in 7 databases. More than 25,000 differentially expressed genes (DEGs) according to FPKM were upregulated or downregulated. We observed 221 and 850 DEGs at 2 and 4 dpi, respectively, in BRV-infected microshoots related to the stress response. The proportion of upregulated DEGs at 4 dpi was about 3.5 times higher than at 2 dpi. Pathways of the virus defense response were activated, and key candidate genes were identified. The phenylpropanoid and the cutin, suberine, and wax biosynthesis pathways were activated in infected plants. Our comparative de novo analysis of the R. nigrum transcriptome provides clues not only for understanding the molecular BRV resistance mechanisms but also for breeding BRV-tolerant genotypes.