The bacterial foodborne pathogen clonal complex 1 (-CC1) is the most prevalent clonal group associated with human listeriosis and is strongly associated with cattle and dairy products. Here, we analyze 2021 isolates collected from 40 countries, covering -CC1 first isolation to present days, to define its evolutionary history and population dynamics. We show that -CC1 spread worldwide from North America following the Industrial Revolution through two waves of expansion, coinciding with the transatlantic livestock trade in the second half of the 19th century and the rapid growth of cattle farming and food industrialization in the 20th century. In sharp contrast to its global spread over the past century, transmission chains are now mostly local, with limited inter- and intra-country spread. This study provides an unprecedented insight into phylogeography and population dynamics and highlights the importance of genome analyses for a better control of pathogen transmission.