After law school, Hamline began practicing law in Evanston, Illinois where he was elected as village attorney several times. He married Josephine Meade of Norwich, New York in 1880. In 1883, he moved to Chicago. He was elected to the Chicago City Council in 1887 as alderman for the Third Ward, holding that position until 1889.
Hamline died on February 14, 1904.
John H. Hamline Elementary School in Chicago is named in his honor.
- "John H. Hamline Dead: A Well-Known Chicago Lawyer and Champion of Civil Service Reform" (PDF). The New York Times. February 15, 1904.