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The land across the harbour from Sydney was originally inhabited by the Cammeraygal tribe of the Guringai nation before land grants in the area were taken up in the 1820s. Named after the area's first land owner Edward Wollstonecraft in 1825, the remoteness of the lower north shore saw only minor settlement in the harbour-fronted suburb. Those who did settle in Wollstonecraft were variously wealthy business owners from Sydney who sought the isolation offered in the suburb or workers from harbourside industry located in nearby McMahons Point.
With the completion of the Harbour Bridge and subsequent railway line linking Wollstonecraft to Sydney in 1932, suburbs which had previously been mainly accessible by boat on the harbours northern foreshore such as Wollstonecraft would experience significant residential growth. The subdivision of larger land blocks and residential development of this time can be seen from the dominance of Californian Bungalows in the suburbs streets. The picturesque suburb continues as a popular suburb with residential developers and high density housing comprises the majority of housing in Wollstonecraft today.