He played nine seasons in Major League Baseball (MLB) between 1949 and 1960 for the Chicago Cubs, Brooklyn Dodgers, Washington Senators, New York Giants, and Kansas City Athletics.

He joined the Marines in 1943 following his 18th birthday and served as a radioman on an amphibious tank in the Pacific Theater of World War II.

[3] In 1948, after finishing college, Terwilliger was playing second base with the semi-pro Benton Harbor Buds when he was signed as a free agent in July by the Chicago Cubs.

[3] Terwilliger spent the 1950 season as the Cubs' starting second baseman, hitting .242 with 10 home runs, 32 RBI, and 13 stolen bases.

[5] However, after getting off to a poor start to the 1951 season, Terwilliger was included in a trade that sent outfielder Andy Pafko, pitcher Johnny Schmitz, and catcher Rube Walker to the Brooklyn Dodgers for catcher Bruce Edwards, pitcher Joe Hatten, outfielder Gene Hermanski and infielder Eddie Miksis.

[4] After starting the 1960 season with the A's, Terwilliger was unofficially traded to the New York Yankees, a transaction that was common at the time between the two teams when the Yankees were accused of using the A's as a major league farm club and the two teams often seemed to have mutual rights to each other's players,[6] and played the rest of the season at AAA Richmond Virginians before retiring as a full-time player.

[11] Terwilliger returned as a major league coach after being hired to Don Zimmer's 1981 Rangers staff and would stay with the team for four years.

[4] He would stay on with rookie manager Tom Kelly, handling the job when the team won the World Series in 1987 and 1991 before leaving following the 1994 season.

[12] Staying in Minnesota, Terwilliger returned to the St. Paul Saints in 1995, this time as the first-base coach of the team in the independent Northern League.