Watkins was born in De Queen, Arkansas but moved to Oklahoma as a boy. He graduated from Oklahoma State University in 1960, receiving a master's degree from that same school in 1961. After a brief stint working for the USDA, he worked as an administrator at his alma mater from 1963 to 1966 Later, he spent two years heading one of the first economic development districts in the country, based in Ada.

Watkins became active in Democratic politics in the early 1970s, and was elected to the state senate in 1974. Two years later, U. S. House Speaker Carl Albert announced his retirement after 30 years representing Oklahoma's 3rd Congressional District. The district was based in the southeastern part of the state, known as Little Dixie, and was heavily Democratic. Watkins gained Albert's endorsement and won with 82f the vote. He was reelected six more times, always by close to 80f the vote. For most of this time, he served on the Budget or Appropriations Committees, allowing him to bring large amounts of money to his mostly agricultural district. He was also very active in oil and natural gas issues.

Watkins didn't seek an eighth congressional term in 1990, but instead ran for the Democratic nomination for governor. He lost to eventual winner David Walters, whose campaign's tactics so enraged Watkins that he ran for governor again in 1994, this time as an independent. He only won 23f the vote. However, he siphoned off enough votes from Lieutenant Governor Jack Mildren, the Democratic candidate, to allow Frank Keating to become only the second Republican governor in Oklahoma history.

In 1996, Bill Brewster, who succeeded Watkins in the 3rd District, decided to retire. Watkins made no secret of his desire to get his old seat back. He finally decided to run as a Republican after that party's leadership promised him a seat on the Ways and Means Committee if he won. No congressman had ever served on all three of the major financial committees (Appropriations, Budget and Ways and Means) before. Despite Albert endorsing Watkins' Democratic opponent, Watkins won a narrow victory--the first competitive race in the 3rd District in decades. He became the first Republican to represent Little Dixie since Oklahoma joined the Union in 1907. He initially planned to retire for good in 1998 after undergoing brain surgery, but was persuaded to run again. He was handily reelected that year and faced no major-party opposition in 2000. Watkins' voting record in his first period in Congress had been somewhat moderate, but during his second term it was staunchily conservative.