Salmonella enterica is a ubiquitous and clinically-important bacterial pathogen, able to infect and cause different diseases in a wide range of hosts. Here, we report the isolation and characterization of a new S. enterica serovar (13,23:i:-; S. Tirat-Zvi), belonging to the Havana supper-lineage that was isolated from a wild house sparrow (Passer domesticus) in Israel. Whole genome sequencing and complete assembly of its genome indicated a plasmid-free, 4.7 Mb genome that carries the Salmonella pathogenicity islands 1–6, 9, 19 and an integrative and conjugative element (ICE), encoding arsenic resistance genes. Phenotypically, S. Tirat-Zvi isolate TZ282 was motile, readily formed biofilm, more versatile in carbon source utilization than S. Typhimurium and highly tolerant to arsenic, but impaired in host cell invasion. In-vivo infection studies indicated that while S. Tirat-Zvi was able to infect and cause an acute inflammatory enterocolitis in young chicks, it was compromised in mice colonization and did not cause an inflammatory colitis in mice compared to S. Typhimurium. We suggest that these phenotypes reflect the distinctive ecological niche of this new serovar and its evolutionary adaptation to passerine birds, as a permissive host. Moreover, these results further illuminate the genetic, phenotypic and ecological diversity of S. enterica pathovars.