Hawkins was born in Plymouth. He led extremely profitable expeditions on the west African coast to capture slaves. Hawkins pretended to betray Queen Elizabeth I in 1571 by offering his services to the Spanish, in order to obtain the release of prisoners and to discover plans for the proposed Spanish invasion of England.
In 1571 Hawkins entered Parliament and became treasurer (1573 - 1589) and comptroller of the navy. He made important improvements in ship construction and rigging. In the defeat of the Spanish Armada (1588), Hawkins commanded the HMS Victory and was knighted for his services.
In 1595 he accompanied Francis Drake on a treasure-hunting voyage to the West Indies, during which he died at sea off Puerto Rico.