The United States Postal Service has organized these 36 places into 30 five-digit ZIP Codes, served by 20 post offices.

Near this hamlet, in the village of Cove Neck, is Sagamore Hill, the former residence and summer White House of U.S. President Theodore Roosevelt and now a museum.

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.

In 1639, the Dutch West India Company made its first purchase of land on Long Island from the local Native Americans.

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.

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.

"[4] 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.

In 1918, Glen Cove, to the west, incorporated as a city and formed a governing system separate from the town.

[7] There are 40 buildings and sites presently named Town of Oyster Bay Landmarks.

[8] The 2019 American Community Survey determined the population was 293,576, estimating a 1.6% increase from the 2010 United States census.

Aer Lingus operates its United States office in Oyster Bay, centered on the hamlet of Jericho.

[14][15][16] Cablevision Systems, a major cable company in the tri-state area has its corporate headquarters in Bethpage, New York,[17] as well as a satellite office in Jericho, New York that contains its medium to large business solutions division, Lightpath.

LIU Post, the largest campus of the private Long Island University system, is located in Brookville.

The Main Line runs through the center of the town from with stations in Hicksville, and Bethpage.