The Japanese beetle (Popillia japonica), native to Japan, is a major invasive species in North America and Europe. Its colonization of Europe began on the Azores (1970s), followed by Italy (2014) and southern Switzerland (2017). In 2023, the presence of the pest was reported in three areas of Switzerland: Kloten (Canton of Zürich, north-eastern Switzerland), Basel (Canton of Basel-Landschaft, northern Switzerland), and in eastern Canton of Valais (South Switzerland) near the Italian border. In 2024, P. japonica individuals were discovered in several other Swiss Cantons. To trace P. japonica spread and origins in Switzerland, we investigated 42 individuals from infested areas, comprising scattered findings across Switzerland. Phylogenetic and population structure analyses using whole-genome resequencing, including data of previously sequenced samples from Japan, North America, the Azores, Italy, and Southern Switzerland, revealed distinct P. japonica migration patterns. Populations in Basel, Valais, and central Switzerland likely originated from Ticino/Northern Italy via road or rail transport. Conversely, the population near Zürich Airport was identified as an independent introduction from North America, likely through unintentional air transport. These findings offer insights into P. japonica spread across Switzerland, highlighting the need for enhanced monitoring and identification of invasion pathways.