While studying to become a lawyer, he worked for his uncle, John Fairfield and graduated from Harvard in 1840 with an LL.B. He was awarded an honorary degree of A. M. from Bowdoin College in 1860.He practiced law in Boston, Massachusetts. John Wingate Thornton researched and wrote numerous family genealogies and authored a number of books. In 1844 he was a founding member of the New England Historic and Genealogical Society and authored numerous articles for their publication, the Register. He was a member and Vice-President of the American Statistical Association, a member and Vice-President of the Prince Society, and a member of the American Antiquarian Society.
His 1844 report to the American Statistical Association was presented to Congress by John Quincy Adams who notes that it demonstrates "a multitude of gross and important errors in the printed census of 1840."
In August of 1607, a company of Englishmen were landed near the mouth of the Kennebec River in Maine with the intent of starting a colony known as the Popham Colony. However, half of the colony returned in December of 1607 and the remaining members returned to England the following year. John Wingate Thornton was invited to deliver a speech on August 29, 1862, during an occasion set to commemorate the failed Popham Colony. Much to the chagrin of the audience and Fort Popham Celebration committee members, John Wingate Thornton correctly pointed out, in contradiction to the beliefs of those who invited him, that the Popham Colony was not the first attempt at New England colonization, and that additionally it was not a serious attempt at creating a permanent colony as only men and not entire families were sent. His unpopular speech was left out of the printed proceedings of the commemoration and John Wingate Thornton resorted to privately printing the text of his speech in 1863.
He died on June 6, 1878 at the Oak Hill family estate in Scarborough, Maine and is buried in the Laurel Hill Cemetery in Saco, Maine.
On May 31, 1848 he was married to Elizabeth Wallace Bowles by the Reverend Augustus C. Thompson in Roxbury, Massachusetts. They had four children, only one of whom (Elizabeth Thorndike Thornton)survived to adulthood.