In most growing countries, apricot (Prunus armeniaca L.) was regarded as self-compatible. Seven incompatibility S-RNase alleles were detected among North American and Mediterranean cultivars and one (SC) was clarified to be responsible for the self-compatible phenotype. The SC-haplotype was shown to be a naturally occurring pollen-part mutant of S8, first time detected in a Hungarian genotype. Only two cross-incompatibility groups (CIGs) were established and a restricted variability in the S-locus of apricot was reported. Our analyses revealed a much abundant allele pool. We have described 13 new S-RNase alleles from East European and Asian genotypes. Mutations were also found within the S-RNase gene of some haplotypes, which allowed monitoring crop evolutionary connections among different geographical groups of P. armeniaca cultivars. An extended analysis of Turkish apricot germplasm has revealed the presence of two additional S-RNase alleles and 12 novel CIGs, making apricot more similar to some incompatible Prunus species. Allele mining from Turkish and Hungarian apricots and the detection of shared allele pools furnished molecular evidence supporting the long-suspected historical connection between Hungarian and Turkish germplasm. This connection appeared to be relatively recent and associated with historical events dating back 300 years rather than coinciding with primary dissemination routes of apricot from Central Asia to Europe dating back 2000 years, as previously believed. Our results suggest that the mutation rendering the apricot S C-haplotype non-functional might have occurred somewhere east of Central Turkey. In other studies, approximately 50 S-RNase alleles were identified from Chinese apricot cultivars using different marker systems (isoelectric focusing, PCR and sequencing). Our in silico comparison of the available S-RNase alleles clarified that those detected in the Chinese cultivars were rather different from those in the Central Asian and European apricots. These data highlight the need of harmonization.