Abstract The self‐replicating polerovirus‐associated RNAs have recently been classified as tombusvirus‐like associated RNAs (tlaRNAs). In a metagenomic comparison of the virome of wild ( Daucus carota subsp. carota ) and cultivated ( D . carota subsp. sativus ) carrots, four tlaRNAs were identified: carrot red leaf virus‐associated RNA (CtRLVaRNA), beet western yellows virus‐associated RNA (BWYVaRNA), and two other tlaRNAs detected for the first time in carrots, arracacha latent virus E‐associated RNA (ALVEaRNA) and a new tlaRNA tentatively named carrot red leaf virus‐associated RNA 2 (CtRLVaRNA‐2). Their genomic sequences show a typical tlaRNA genome organization with a very short 5′ untranslated region (UTR), a long 3′ UTR and consecutive open reading frames (ORFs), ORF1a and ORF1b, separated by an amber stop codon, leading to the production of an ORF1a/ORF1b RdRp fusion protein. The genetic diversity and prevalence of these various agents were analysed in carrot populations in France and Spain. CtRLVaRNA was the most frequently detected in both wild and cultivated carrot populations and was genetically more heterogeneous than ALVEaRNA and CtRLVaRNA‐2. ALVEaRNA was detected both in France and Spain and showed preferential association with cultivated carrots. In contrast, CtRLVaRNA‐2 was only detected from one region of France and was preferentially associated with wild carrot populations. Analysis of the virome of individual plants showed the presence of CtRLV but not that of the expected helper virus for ALVEaRNA and BWYVaRNA, suggesting a degree of flexibility in their associations with helper viruses, which in turn may have biological and epidemiological consequences.