John Motley Morehead III's cousin, John Lindsay Morehead II, is fondly recalled as the "architect" of the Morehead Program. John Lindsay Morehead designed and implemented the intricate Morehead selection process that is still in place today. He was a cherished advisor to John Motley Morehead throughout his life and served as the inaugural vice chairman of the Morehead Foundation Trustees.

Born October 19, 1894, John Lindsay Morehead was graduated from the University of Virginia in 1915. He worked for his family's business, the Leaksville Woolen Mills, Inc., and upon his father's death in 1923 became president of the company. In addition, he was president of Brunswick Navigation Corporation, a fisheries company.

John Lindsay Morehead and his wife, Louise Nickerson Morehead (1893-1976), had three daughters:

• Mary Nickerson Morehead Chatham (1921-1990), whose husband, Hugh G. Chatham, was a Foundation Trustee from 1950 to 1985 (chairman from 1967 to 1985). Their daughter, Lucy Hanes Chatham, is currently the vice chairman of the Foundation Trustees.
• Jean Motley Morehead Larkin (1928-), who served on the Foundation Board of Trustees from 1984 to 2004.
• Louise Lindsay Morehead Dickson (1931-1988), whose husband, Alan T. Dickson, has been on the Board of Trustees since 1965 and is currently its chairman.

John Lindsay Morehead died November 9, 1964.