John was born in Derbyshire, England in 1592, and was baptized at the Church of All Saints in Derby on July 14, 1592. A follower of the Puritans from an early age, he emigrated to Massachusetts Bay Colony with his wife, children, and sister in 1623. As a trader he sailed to Virginia and England, but by 1630 he was back in the Bay Colony.
He took up residence on an island in the Charles River and was a member of the church at Watertown. Oldham represented Watertown in the colony's first General Court or assembly in 1634. He continued in the Indian trade, sailing the coast from Maine to New Amsterdam.
In July of 1636 he was on a voyage to trade with Indians on Block Island. On July 20 he was boarded by hostile Indians, presumed to be Pequots. He and five of crew were killed, and two young boys with him were captured. The ship's cargo was looted. A fishing vessel rescued the boys and tried to tow his sloop to port. When adverse winds affected them, they scuttled the ship but brought the two boys home. The Bay Colony was outraged at this latest incident, and sent John Endicott with a force to retaliate.