To efficiently protect the integrity of genetic information, transcription is connected to nucleotide excision repair (NER), which allows preferential repair of the transcribed DNA strands (TS). As yet, the molecular basis of this connection remains elusive in eukaryotic cells. Here we show that, in haploids, the RAD26 gene is essential for the preferential repair of the TS during G1. However, in G2/M phase there is an additional RAD51-dependent process that enhances repair of TS. Importantly, the simultaneous deletion of both RAD26 and RAD51 led to complete abolishment of strand-specific repair during G2/M, indicating that these genes act through two independent but complementary subpathways. In diploids, however, RAD51 is involved in repair of the TS even in G1 phase, which unveils the implication of homologous recombination in the preferential repair of the TS. Importantly, the abolishment of NER, by abrogation of RAD1 or RAD14, completely stopped repair of UV damage even during G2/M phase. These results show the existence of functional cross-talk between transcription, homologous recombination and NER.