He was a Democrat, and began his political career at the age of 21 serving on the Putnam City Council. He later served as mayor of Putnam, before being elected to Governor of Connecticut. In 1925, the family moved to Putnam, Connecticut, in the northeastern corner of the state.
He worked there in the textile industry and then in the Town Hall, which made the start for his rise in state politics.
While living in Putnam, Dempsey was the Soccer Coach at the Pomfret School in Pomfret. In 1936, at the age of 21, Dempsey was elected to the Putnam City Council, and in 1948, he began the first of six terms as mayor.
He was elected to the Connecticut House of Representatives in 1949, but managed to divide his time between state and local affairs He served in the General Assembly until 1955, when he became executive secretary of governor Abraham A. Ribicoff.
Dempsey was the 74th Lieutenant Governor of Connecticut during Ribicoff"s last term as governor, from 1959-1961.
Dempsey succeeded him becoming the first person to hold this position since the early colonial period who had been born in Europe. Both houses voted unanimously to override his veto, and the General Assembly emerged as a co-equal branch of government. He chose not to run for re-election in 1970 and was succeeded by Republican Thomas J. Meskill.
During his tenure, he served on the Advisory Commission on Intergovernmental Relations, the National Governors Association Executive Committee from 1968 to 1969.
Also chaired the New England Governors Association from 1963 to 1965 and the Democratic Governors Association from 1969 to 1970. After leaving office, Dempsey became the President of the Indian Trails Council of the Boy Scouts of America.
The University of Connecticut Health Center in Farmington, Connecticut is known as John Dempsey Hospital. He was treated for lung cancer there himself in the last month of his life.
He died in his home, on July 16, 1989 (age 74 years, 194 days) at Killingly Center, Windham County, Connecticut.
He is interred at Saint Mary Cemetery, Putnam, Windham County, Connecticut.
In 1969, leaders of both parties introduced the Legislative Management Acting to establish support staff and control the operating budget of the Assembly.
When Ribicoff resigned as Governor of Connecticut to become a member of President John F. Kennedy"s Cabinet.