An outbreak of salmonellosis in wild passerines caused mass mortality of Eurasian Tree Sparrows (Passer montanus) in Hokkaido, Japan, 2005–06; however, the etiology was poorly understood. In winter 2008–09, sparrow mortality again occurred in Hokkaido, and 202 deaths in 100 incidents at 94 sites were reported. We conducted a comprehensive investigation to evaluate the cause and impact on sparrow populations. We collected 26 carcasses at 13 sites, including a zoological park. In addition, Salmonella screening of zoo animals was conducted as a biosecurity measure. Salmonella Typhimurium was isolated from multiple organs in all examined sparrows; they were diagnosed with septicemic salmonellosis. Eleven sites (85%) were related to wild bird feeding and six of eight sparrow fecal samples, including from the zoo, were S. Typhimurium-positive. No infection was detected in zoo animals. Isolates belonged to three phage types: DT40 (88%), DT110 (8%), and DT120 (4%). Pulsed-field gel electrophoresis patterns were the same in all isolates, regardless of phage type. Biochemical characteristics and antibiotic-resistance profiles of DT40 were similar in all isolates, indicating a single origin. The mortality was likely associated with that in 2005–06 because the isolates had the same profiles. Tissue levels of sodium, calcium, and magnesium (the main components of chemical deicer suspected to be the major cause of poisoning deaths in 2005–06 mortality) were not higher in the affected sparrows. We conclude that an emerging epidemic infection with S. Typhimurium DT40 related to bird feeding was the cause of sparrow mortality in 2008–09 and suggest that this causative strain is host-adapted to sparrows in Japan. The mortality might have had some impact on the local population, but its influence was limited.