Elephant endotheliotropic herpesviruses (EEHVs) cause an acute haemorrhagic disease (HD) in juvenile Asian elephants (Elephas maximus), referred to as EEHV-HD. This disease is fatal in up to 80% of cases even with intensive supportive care. Since the virus discovery, no studies have explored the genetics contributing to the diversity of EEHVs. So far seven genotypes of EEHV have been assigned using limited sequence data but without consensus on candidate genes for phylogenetic, epidemiological, or evolutionary analysis. Additionally, no animal or cell culture model is available to study the pathogenesis of EEHV infection or to assess the antiviral potential of drugs. This study aimed to sequence and characterise EEHV-1A/B strains detected in Asian elephants held in Europe, harmonise phylogenetic and epidemiological analysis of the viruses, discover intra- and inter- specific genetic variations and establish a cell culture model for EEHV-1. Thirteen new EEHV-1 coding sequence (CDS) were obtained from elephants of six zoological collections. Phylogenetic analysis revealed two clusters within EEHV-1A. All collections possessed their own unique strain(s) of EEHV-1A, more than one strain in a larger collection and identical strains in fatality pairs. The EEHV-1A nucleotide identity at the CDS level was 93.8-100%. Nine genes were used to harmonise phylogenetic and epidemiological studies with comparable outcome to that of the CDS. Evolutionary analysis confirmed the role of recombination events and single nucleotide polymorphisms (SNP) for genetic diversity. However, no pathogenicity markers could be determined due to limited cases of survivor and asymptomatic animals. Attempts to isolate EEHV-1A in cell culture proved inconclusive, however, evidence warrant further investigation in 3T3 cells and chemicals modifying the host cell status.