Various grottos were dug into the rocky hillside descending from north to south, and were used as part of the home or for production systems. Among these, only two were part of the Shrine: one larger version, venerated for the Annunciation, and a smaller and irregular one known as the Grotto of Conon. The grottos underwent several changes above all in the Middle Ages, when the grotto of the Annunciation was expanded and that of the Conon was partially demolished and set underground. However, it is quite plausible that from the very start their form would have been changed on insertion within the place of worship.
Today the grotto of the Annunciation features an irregular layout, running 5.5 metres from north to south and 6.14 metres from west to east, with a small apse in the eastern wall. Of the Byzantine era, there are remains on the northern side of layers of plaster, which in all likelihood covered the entire bare rock face of the Grotto. Another interesting feature, in the second layer, is a number of traces of graffiti.
The second grotto, known as the grotto of Conon, may once have been used as a memorial space with a raised bench. This area was set underground in the Middle Ages. On the eastern wall there are a remarkable six layers of overlaid plaster. The oldest plaster can now be seen, representing a strip with flowered plants and crown, and a painted inscription in Greek. According to Bagatti and Testa the painted inscription names Valeria “servant to our Lord Christ”, who made “a memory for the light”, in other words had the grotto decorated with the representation of a flowered Heaven in memory of a martyr, perhaps the same Conon of Nazareth. There are other examples of graffiti in the plaster, with a series of names and entreaties to Christ; a coin dates this oldest layer of plaster to the second half of the 4th century.