We studied the mode of pollination in Greek oregano (Origanum vulgare ssp. hirtum) under both controlled and open pollination conditions. When grown indoors without the presence of insects, Greek oregano plants did not develop any seeds, indicating a low level of spontaneous self-pollination. Applying manual self-pollination under the same conditions resulted in only 16 seeds, of which only five were able to germinate. At the same time, a clonally propagated Greek oregano plant of the same genotype produced a rich set of over 300 seeds in open field conditions when the flowers were visited by insects in an area where no other Origanum species were observed. Analysis with SSR markers showed that over 70% of the seeds likely resulted from self-pollination, indicating that insect-mediated pollination is essential for the seed development. We further analyzed the cross-pollination of Greek oregano with Common oregano (O. vulgare ssp. vulgare) in open field conditions where the two subspecies were grown in close proximity. Applying SSR markers, we analyzed 83 plants obtained from seeds of three vegetatively propagated Greek oregano mother plants. Surprisingly, the results showed that all analyzed seedlings resulted from cross-pollination of Greek oregano with Common oregano, indicating that cross-pollination between the two subspecies can completely take over the self-pollination or cross-pollination between the Greek oregano plants. The possible impact of the observed high cross-pollination rate on the genetic origin of seeds of selected Greek oregano lines and varieties, as well as on the genetic diversity and structure of natural populations, is discussed.