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Succeeding cultures of indigenous peoples had lived in the area for thousands of years. At the time of European contact, the Lenape (Delaware) nation inhabited western Long Island. By 1600 the band inhabiting the local area was called the Matinecock after their location, but they were Lenape people.

Following European colonization, the area became part of the colony of New Netherland. In 1639, the Dutch West India Company made its first purchase of land on Long Island from the local Native Americans. The English also had colonies on Long Island at this time. The Dutch did not dispute English claims to what is now Suffolk County, but when settlers from New England arrived in (present-day) Oyster Bay in 1640, they were soon arrested as part of a boundary dispute. In 1643, Englishmen purchased land in the present-day town of Hempstead from the Indians that included land purchased by the Dutch in 1639. Nevertheless, in 1644, the Dutch director granted a patent for Hempstead to the English.

The Dutch also granted other English settlements in Flushing, Newtown, and Jamaica. In 1650, the Treaty of Hartford established a boundary between Dutch and English claims at “Oysterbay”, by which the Dutch meant present-day Cold Spring Harbor (to the east) and the English meant all of the water connected to present-day Oyster Bay Harbor. Meanwhile, the government of England came under the control of Oliver Cromwell as a republic, and smugglers took advantage of the unresolved border dispute. In 1653, English settlers made their first purchase of land in Oyster Bay from the local Matinecock tribe, though there were already some rogue English settlements there. For this purchase, the English settlers paid to the Native American Moheness (aka Assiapum), “six kettles, six fathoms of wampum, six hoes, six hatchets, three pairs of stockings, thirty awl-blades or muxes, twenty knives, three shirts and as much Peague as will amount to four pounds sterling.” The monarchy was restored in England in 1660, and in 1664 King Charles gave Long Island (and much else) to his brother James, leading to the Dutch relinquishing control of all of New Amsterdam.