St. John of Doves began as a single tower erected by fighters from the Fourth Crusade in 1203 A.D. to guard against pirate invasions from the beach below (which forms a natural harbor). The site probably was chosen because of the spring that still runs freely from a point near the base of the tower, and for its unobstructed views of the coastline and the channel running between Corfu and the mainland. According to tradition, carrier pigeons were bred on the site to carry news of danger to the Venetian fort in Corfu Town.

After the fall of Byzantium in the 15th Century, other buildings were added (including the house, the church, and the olive press), and 2600 olive trees were planted. These and more olive trees continue to flourish on the estate. During the Venetian occupation of Corfu, which ended in the 18th Century, the estate was used as a monastery, and the property retains its calm and peaceful atmosphere to this day.

The first mention of the name of the estate's private owners appears in a Venetian document dated July 29, 1669. The document shows that the property was acquired by the famous Theotoki family, one of Corfu's most wealthy and prestigious families. The estate remained in the Theotoki family until 1894, and their family crest continues to be associated with the estate. The crest shows a lion holding a sword, and stepping on its vanquished enemy.

The private chapel is consecrated to St John the Baptist. A report prepared by the Greek Orthodox Church in 1754 identifies the chapel, and carefully catalogues its contents at the time. During the occupation of Corfu by Napoleon's troops in 1798, however, the chapel's frescoes were partly destroyed and its contents removed. The frescoes could be restored. The church was closed until 1809, when it was restored to the Theotoki family and reopened with its current contents (including the altar, icons, incense lamps, and wooden stacidia). The chapel is recognized by the Greek Orthodox Church, and may be used for weddings and other religious ceremonies to this day.

The current owners' family acquired the estate in 1922, when the statesman Constantine Zavitzianos purchased it for use as a working farm and summer estate. Mr Zavitzianos was one of the early members of parliament under the newly independent Greek government, serving as Corfu’s representative in the national government for 40 consecutive years. He also served as Speaker of the House twice under the famous prime minister E. Venizelos (after whom the Athens International Airport is named), as well as in the position of Vice President of Greece.

The house last was used by the current owners' family as a refuge from the massive bombings suffered by Corfu during World War II.