Long before any European arrived, the Coree people lived along this stretch of coast - Algonquian-speaking Native Americans who left behind a great mound of oyster shells at Shell Point on the eastern end of the island. The Core Sound and Core Banks both still carry their name. In 1584, an expedition financed by Sir Walter Raleigh charted these waters for the first attempted English colony in North America; the explorers brought two Native Americans back to England, including a man named Wanchese whom local island legend identifies as a Coree from Harkers Island. The island appeared on a 1624 map drawn by Captain John Smith as "Davers Ile," probably named for Sir John Davers, one of the founders of Jamestown. By the time Ebenezer Harker bought what was then called Craney Island on September 15, 1730, for £400 and one twenty-foot boat with oars and mast, the Coree were already mostly gone. The island became known by his name within a generation.

Ebenezer Harker had come from Massachusetts by way of Wales, made his way into the whaling trade, and arrived in Beaufort by 1728 to collect whale oil taxes. He built a plantation and boat yard at the western end of the island and raised an extended family of three sons, two daughters, and at least nine enslaved Africans. When he died in 1762, his will divided the island and the people among his children. His son Zachariah inherited the western third along with two enslaved people: an adult woman named Vilet and a young girl named Daisie. James inherited the eastern third and two more: an adult woman named Hague and a young boy named Peter. Ebenezer Jr. inherited the middle third along with Jeffrey and Sutton. Daughter Sarah Freshwater received a woman named Hope. The will left the fate of an elderly enslaved woman named Badge and a young boy named Ben for the heirs to decide. The names survive because the will survives. The people who carried them - their lives, their families, their work - built much of what Harkers Island became, and the historical record gives us little beyond their names and the property categories in which they were listed.

In 1899, a series of hurricanes tore through the Outer Banks villages - especially Diamond City on Shackleford Banks - and the survivors fled inland. Many landed on Harkers Island, more than doubling the population and giving the island the distinctive Banker-descended families that shaped its modern culture. A post office opened in 1904. The first paved road across the island, Harkers Island Drive, went down in 1926 - paved, in a small touch of historical irony, with oyster shells dug from the old Coree mound at Shell Point. Until 1941, residents reached the mainland only by ferry. That year a wooden drawbridge opened across the narrow channel to the small town of Straits, despite local complaints that a bridge to Beaufort would have made more sense for commerce and hospital access. (The bridge was later replaced by a steel span in 1968 and named the Earl C. Davis Memorial Bridge in 1991.) In November 1941, construction began thirty miles northwest on a new Marine Corps air station at Cherry Point, bringing wage jobs to local workers. Within weeks the United States was at war, and German submarines patrolled visibly off the coast. Island residents could stand on the beach at night and watch the tankers burning offshore.

Harkers Island has one of the highest concentrations of Latter-day Saints anywhere in North Carolina - a result of Mormon missionaries who arrived in the late 1890s and converted whole families in a region that was otherwise solidly Baptist and Methodist. The first school on the island opened in 1864 when a teacher named Miss Jenny Bell came down from Boston, sponsored by the Northern Methodist Episcopal Church. Today the island's largest cultural institution is the Core Sound Waterfowl Museum and Heritage Center - a 20,000-square-foot building on land leased from the National Park Service, dedicated to the long tradition of decoy carving that grew out of waterfowl hunting on Core Sound. The Decoy Festival and Waterfowl Weekend, held the same weekend each year, are the island's biggest annual events. The carvers' guild meets year-round. The work of the old masters fills cases in the museum, alongside exhibits on the dialect, the families, the storms, the bridge, and the long slow arc of an island that took nearly two centuries to connect itself to the mainland.

When the federal government created Cape Lookout National Seashore in 1966, taking in the Core Banks and Shackleford Banks just south of Harkers Island, it brought turmoil. Generations of Harkers Island fishermen had built cottages on the Banks - often without clear title, on land where shorelines moved and surveys disagreed. Few owned what they thought they owned. Legal eviction proceedings dragged on into the 1980s. The Park Service ended open grazing on the Banks by December 31, 1985. In late December of that year, a series of arson fires destroyed most of the major structures on Shackleford Banks, including a newly built park visitor center. An FBI investigation never identified the arsonists. The Shackleford wild horses - allegedly descended from Spanish shipwrecks in the sixteenth century - were allowed to remain. The cottages were not. Today the visitor center for the entire seashore sits on Harkers Island itself, a quiet acknowledgment that whatever happens out on the Banks, the island remains the gateway.