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In 1939, he was appointed first assistant clerk of the [[Vermont House of Representatives]], and he served until 1941.{{sfn|"Parker Named Ass't House Clerk"}}{{sfn|''Vermont Legislative Directory''}} In 1943 he was elected Clerk of the House as the replacement for [[Harold J. Arthur]] during Arthur's military service for [[World War II]].{{sfn|"Asa S. Bloomer Elected Speaker of the House"}}{{sfn|"List of Clerks of the Vermont House of Representatives"}} Parker served as Clerk until 1947, when he was succeeded by Arthur.{{sfn|"List of Clerks of the Vermont House of Representatives"}}
In December 1941 he accepted [[Alban J. Parker]]’s (no relation) appointment as Vermont’s deputy attorney general, and he served until the end of Parker’s term in 1947.{{sfn|"Clifton Parker is Named Deputy Attorney General"}}{{sfn|''Vermont Legislative Directory''}} In 1946, Clifton Parker was the successful Republican nominee to succeed Alban Parker.{{sfn|"Clifton Parker Today Becomes Attorney General"}} He was reelected in 1948 and 1950, and served from 1947
He was active in the Vermont Bar Association, and served as its president from 1959 to 1960.{{sfn|"Past Presidents of the Vermont Bar Association"}} In addition, he was a member of the state Board of Bar Examiners for several years.{{sfn|''Vermont Legislative Directory''}} Parker was also active in local government for both Morrisville and [[Morristown, Vermont|Morristown]], including serving on the water and power commission, town attorney, and [[Moderator (town official)#Vermont|town meeting moderator]].{{sfn|"Obituary, Clifton Parker"}}
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