Even before colonial times, Oyster River was of great value to mankind because of the unique environment it created for oysters to breed. The mixture of fresh water from the river and salt water from Long Island Sound allows for the perfect habitat. For Native Americans, the mouth of Oyster River provided a valuable food source. The Native Americans would travel to Oyster River and along the beach dig large holes in the sand allowing them to fill with water. Next they would build a fire on the top of rocks and these heated rocks would be pushed into the water. The Native Americans would then place oysters in the heated water to cook. There were several Native American tribes that lived in the vicinity of Oyster River. The Quinnipiacs occupied New Haven and the Wepawaugs lived around the Milford area.

When the settlers first arrived in New Haven, they lived among the Native Americans. On November 24, 1638, an agreement was reached between the colonists, headed by John Davenport and Theophilus Eaton and Momauguin, the sachem of the Quinnipiac tribe to buy the land that Native American’s possessed in exchange for goods and the assurance that they would be free to hunt and fish the lands. This practice continued for many years. In 1645 the colonists made a purchase with the Native Americans adding the Milford area to the New Haven colony. The first transaction provided land that extended into Milford. A second transaction sold land to the settlers of Milford that extended into West Haven.

At first the Native Americans were very pleased with these negotiations because they never considered they owned the land. They viewed the land as something a person used. Overtime however, the Native American’s realized that these negotiations deprived them of their right to utilize the lands. The colonists put up fences, claiming privacy of both land and water bodies. The Oyster River is an example of one of the many areas the Native American’s were restricted from. Promising not to damage English property and not to work on the Sabbath day, the Native American’s requested permission to spend the summer months along Oyster River to harvest the oysters. The Colonists responded with the following conditions; No strange Indians were allowed to live with them, no Indians were allowed to destroy any man’s fence, cut any wood, enter any settlers’ homes without knocking, bear arms in town, or stay late in town. The Indians were also required to kill all of their dogs. The Native American’s, refusing to kill their dogs, were no longer permitted to fish the Oyster River.

Soon after the New Haven colonists laid out their city and built their homes, they turned attention toward dividing up the remainder of land purchased from the Native Americans. The 1645 purchase of land in Milford and the extension into West Haven caused a long dispute amongst the colonist as to who owned what territory. Both Milford and West Haven claimed they had purchased the same land. It was not until 1674 that this dispute was settled by the State Assembly who determined the Oyster River to be the border separating Milford from West Haven. One of the earliest known dwellings along Oyster River was a small house built by Henry Bristol in the 1830’s.

The colonists, who were shown the natural beds by the Native Americans, began harvesting the oysters along Oyster River for market. Around 1860, an man by the name of Homer Smith and his associates brought a house and went into the fishing business on Oyster River. Raising oysters became an extremely important industry. However, this profitable industry came with restrictions. As early as December 1777, a court order forbid the taking of oysters during the months of May through September and prohibited the carrying of shells away from the shore. On April 7, 1828 during a West Haven town meeting it was voted that oysters could not be gathered without a written permit and a committee of six people were established to oversee the harvesting. Violation of this law was penalized by fine.

Oyster River Point was used as a shipping area for cattle sold to the British Army during the Revolution. The Clark family, who lived in the Oyster River area, were Royalists. During this time period Oyster River Point was commonly referred to as Clark’s Point.