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The earliest known inhabitants of Sayville were the Secatogue tribe of the Algonquian peoples.

Sayville was founded by John Edwards (b. 1738) of East Hampton, New York. He built his home, the first in Sayville, in 1761, located at what is now the northwest corner of Foster Avenue and Edwards Street. The house was destroyed by fire in March 1913. Another man, John Greene, settled what is now known as West Sayville in 1767.

The community had no formal name until 1838 when residents gathered to choose a name for their post office, which had opened on March 22, 1837. Until that time, Sayville was known informally as “over south.” The townspeople held a meeting to decide on a name, and after Edwardsville and Greensville tied in a vote, one resident suggested “Seaville”. According to historical accounts, the clerk at that particular meeting did not know how to spell and had to go home and look in an old Bible he had brought from England years before. In the Bible, the word “sea” was spelled “s-a-y”, and “Sayville” became the name he sent to Washington. After the error was discovered, the community sent a letter of protest to Washington D.C.; however, the Postmaster General responded that the name should stay “Sayville”, as there were many “Seaville”s in the world but no “Sayville”s. As a result, the name stuck. The claim is also sometimes made that “in some very old Bibles, the town name is also spelled ‘S-a-v-i-l-l-e'”., It may be noted that until the early 19th Century, it was common in many varieties of English to pronounce “sea” so that it rhymed with “obey”, and thus “Sayville” could have been a phonetic representation of how some speakers would have pronounced “Seaville.”