Leishmania aethiopica
is a zoonotic Old World parasite transmitted by Phlebotomine sand flies and causing cutaneous leishmaniasis in Ethiopia and Kenya. Despite a range of clinical manifestations and a high prevalence of treatment failure,
L. aethiopica
is one of the most neglected species of the
Leishmania
genus in terms of scientific attention. Here, we explored the genome diversity of
L. aethiopica
by analyzing the genomes of twenty isolates from Ethiopia. Phylogenomic analyses identified two strains as interspecific hybrids involving
L. aethiopica
as one parent and
L. donovani
and
L. tropica
respectively as the other parent. High levels of genome-wide heterozygosity suggest that these two hybrids are equivalent to F1 progeny that propagated mitotically since the initial hybridization event. Analyses of allelic read depths further revealed that the
L. aethiopica
-
L. tropica
hybrid was diploid and the
L. aethiopica
-
L. donovani
hybrid was triploid, as has been described for other interspecific
Leishmania
hybrids. When focusing on
L. aethiopica
, we show that this species is genetically highly diverse and consists of both asexually evolving strains and groups of recombining parasites. A remarkable observation is that some
L. aethiopica
strains showed an extensive loss of heterozygosity across large regions of the nuclear genome, which likely arose from gene conversion/mitotic recombination. Hence, our prospection of
L. aethiopica
genomics revealed new insights into the genomic consequences of both meiotic and mitotic recombination in
Leishmania
.