In China, the woolly apple aphid, Eriosoma lanigerum (Hausmann), was first detected as an invasive species during the 1910s to 1930s, restricted to Shandong, Liaoning, and Yunnan Provinces. However, since the 1990s, the pest has spread into many other areas of China. To determine the possible spread routes of the recently established populations, the genetic diversity and genetic structure of 24 populations in 10 provinces were analyzed using eight microsatellite loci. Analyses using STRUCTURE software identified two genetic clusters overall. Three populations from Yunnan and Xinjiang consisted of individuals originating from a single cluster. Nineteen populations from eight northern provinces consisted only of individuals from another cluster, which formed a single large and panmictic population, resembling a distinct “supercolony” in Northern China. The other two populations from Yunnan consisted of individuals from both clusters. The possible routes of spread of the recently established populations of E. lanigerum in China were revealed as follows: 1) the populations in Northern China (including these from Henan, Hebei, Shanxi, Shannxi, Jiangsu, and Gansu) may have been introduced from Shandong or Liaoning Provinces; 2) the populations in Yunnan consisted of an early-established population and a population introduced secondarily from Shandong or neighboring areas, indicating that the population in Yunnan has at least two sources; and 3) the recently established populations of E. lanigerum in Xinjiang might not have been introduced from the “supercolony” in Northern China. Knowledge of these routes of spread is useful for avoiding further dissemination and/or additional introductions.