Settled in 1648, West Haven (then known as West Farms) was a part of the original New Haven Colony. In 1719, it became the separate parish of West Haven, but was still officially a part of New Haven until 1822.

During the American Revolution, West Haven was the frequent launch and arrival point for raiding parties on both sides of the war. On July 5, 1779, the British invaded New Haven Harbor and came ashore in West Haven and East Haven. Thomas Painter, a teenaged militiaman watching for the approaching British ships while standing atop Savin Rock, is depicted on the city seal. The main commercial street, Campbell Avenue, is named for British Adjutant William Campbell, at the time an ensign in the Third Guards, who rescued the Reverend Noah Williston, the local Congregational minister and outspoken revolutionary, from being bayoneted by British and Hessian troopers, after he broke his leg trying to escape his captors. Campbell then ordered the soldiers to help the minister back to the parsonage and had the regimental surgeon set his leg. Campbell is also credited with keeping the troops in reasonably good order during their march through the village and reportedly had two soldiers arrested after a local woman accused them of stealing her jewelry. Campbell was killed hours later atop Allingtown Hill on his way to New Haven by a local farmer-turned defender. Campbell is buried in the Allingtown section of town off Prudden Street. Patriot victims of the invasion are buried in the Christ Church and First Society Cemetery. A historical headstone marks Campbell's approximate gravesite and is maintained by the West Haven Historical Society.

While West Haven again attempted to incorporate as its own town in 1784, that attempt failed, primarily due to the protests of neighboring Milford, which opposed North Milford becoming part of the new town. West Haven and North Milford tried again in 1786 and 1787 with the same result. The two finally joined to become Orange (incorporated as a town in 1822). In 1921, West Haven split from Orange to become a separate town. It was incorporated as a city in 1961 and is known as "Connecticut's Youngest City", but it is ironically one of the state's oldest settlements.

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