Watkins also served as chairman of the Senate Subcommittee on Indian Affairs and championed the termination policy of American Indian tribes. He also was recognized as a reclamation authority and was instrumental of the Deer Creek Reservoir Project. He successfully sponsored both the $760 million Colorado River Storage Act and the $70 million Weber Basin Project Act.

A strong supporter of Eisenhower, he sponsored the Refugee Act of 1953 for the president and served as administration spokesman for civil rights legislation in both the 84th and 85th Congress. In 1958, Watkins was defeated for reelection because of his support for McCarthy's censure and also due to J. Bracken Lee's third-party candidacy, which split the Republican vote and allowed the election of Democratic candidate Frank Moss.