Equine arteritis virus (EAV) is maintained in the horse populations through persistently infected stallions. The aims of the study were to monitor the spread of EAV among Polish Hucul horses, to analyse the variability of circulating EAVs both between- and within-horses, and to identify allelic variants of the serving stallions EqCXCL16 gene that had been previously shown to strongly correlate with long-term EAV persistence in stallions. Serum samples (n = 221) from 62 horses including 46 mares and 16 stallions were collected on routine basis between December 2010 and May 2013 and tested for EAV antibodies. In addition, semen from 11 stallions was tested for EAV RNA. A full genomic sequence of EAV from selected breeding stallions was determined using next generation sequencing. The proportion of seropositive mares among the tested population increased from 7% to 92% during the study period, while the proportion of seropositive stallions remained similar (64 to 71%). The EAV genomes from different stallions were 94.7% to 99.6% identical to each other. A number (41 to 310) of single nucleotide variants were identified within EAV sequences from infected stallions. Four stallions possessed EqCXCL16S genotype correlated with development of long-term carrier status, three of which were persistent shedders and the shedder status of the remaining one was undetermined. None of the remaining 12 stallions with EqCXCL16R genotype was identified as a persistent shedder.