Watkins began his public service career with his election as a judge in the Fourth District Court. In 1932, he was defeated for re-election in Franklin D. Roosevelt's Democratic landslide. After his defeat Watkins immediately began a career in water development. He was instrumental in the organization of various water-users' associations and metropolitan water districts, particularly the Provo River Project.

In 1936. Watkins ran unsuccessfully as a Republican candidate for Congress. Ten years later, he ran successfully for the United States Senate and was reelected in 1952. Watkins became one of the most respected U.S. Senators of his generation and is best known for his service as chairman of the Senate Select Committee which recommended the Censure of Wisconsin's Senator Joseph McCarthy for his conduct in investigating communists in government.