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In 1744, the Teackles settled in the area and built a home at what is today 15 Brooklyn Avenue.
In 1779, the British sloop Thistle came near the town but was forced away from Wachapreague Channel and sunk by fire from forts on Parramore and Cedar Islands.
There was a tidal gristmill in the area located on Mill Creek to the south of town.
It was not until 1874 that Wachapreague began as a small town.
In that year, the Powell brothers sold the first lots to Isaac Phillips and Francis Smith.
By 1883, 15 lots had been sold.
The next year, the town applied for a post office and was denied the name Powellton since this name was already taken.
The town chose the name Wachapreague in its place.

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