Signs and symptoms of a disease similar to those of armillaria root rot have recently been observed on various native woody plants on the foothills of Table Mountain in South Africa, one of the most botanically diverse natural environments globally. This is of concern because the root rot fungus Armillaria mellea has previously been shown to be an alien pathogen of European origin in planted gardens in the City of Cape Town. An aim of this study was to identify the cause of the root rot disease on infected plants. Based on DNA‐sequence phylogeny, it was shown that isolates collected from at least 16 native tree and woody shrub species represented the non‐native A. mellea. Microsatellite markers were then used to determine the genetic diversity and population structure of the A. mellea isolates from Table Mountain and two planted gardens where the pathogen has previously been found. Population genetic analyses revealed low levels of gene diversity and no population differentiation amongst the three populations. The results provide the first firm evidence that A. mellea has escaped the planted environment and invaded a sensitive and ecologically important natural woody environment in South Africa. This is only the second definitive case of a non‐native tree pathogen invading a natural ecosystem in the country.