Tomato (Solanum lycopersicum L.) is an economically important vegetable susceptible to various fungal diseases, including leaf spot caused by Alternaria spp. from the section Alternaria. In our study, a total of 72 tomatoassociated Alternaria spp. strains from Latvia, Lithuania, Estonia, and Algeria were analysed by integrating morphological data, pathogenicity assay, multi-locus phylogeny, and haplotype assignment. Recovered Alternaria spp. strains were characterized by considerable variation in phenotypic diversity, non-pathogenicity to their host of origin and absence of the AAL-toxin biosynthesis gene (ALT1). Multi-locus phylogeny of the RNA polymerase II second largest subunit (rpb2), putative F-box-domain-containing protein (ASA-10), and putative histone-like transcription factor (ASA-19) confirmed the occurrence of both A. alternata and A. arborescens species complexes along with A. longipes and A. postmessia on symptomatic tomatoes. The discordant tree topology among single-gene phylogenies suggested the occurrence of potential recombination between phylogenetic lineages in the section Alternaria, resulting in putative alternata-arborescens and alternata-longipes hybrids. DNA polymorphism analysis of the rpb2, ASA-10, and ASA-19 loci revealed a high level of genetic diversity in the section Alternaria, and the number of single nucleotide polymorphisms (SNPs) and haplotypes varied among loci and lineages studied. A total of 16 and 6 multi-locus haplotypes were assigned in alternata and arborescens lineages, respectively. Global genetic diversity analysis of A. alternata and A. arborescens strains at the rpb2 locus confirmed that major haplotypes described from tomatoes were shared among other hosts of origin.