St. Clair was drafted by the 49ers in the third round of the 1953 NFL Draft. He played his entire 11-year professional career in San Francisco, making his year with the University of Tulsa the only season he did not play home games in Kezar Stadium.
He began his career by successfully holding out for a $6,000 rookie salary. In his first preseason, he earned his spot on the 1953 team by holding his own against defensive tackle Leo Nomellini in practice. Primarily an offensive tackle, he played alongside the Million Dollar Backfield, whose halfback Hugh McElhenny considered him a dominant blocker. He started every game for the 49ers from 1954 to 1956, when he also received his first Pro Bowl selection.
Due to his size, St. Clair was also an effective special teams player. He blocked 19 field goals over the course of his career, ten of which came in 1956, and was instrumental in Abe Woodson's 105-yard kick return touchdown in 1959.
His only postseason game came in 1957. After missing eight weeks with a shoulder injury early in the season, St. Clair returned as the 49ers ended the season with an 8–4 record, tying the Detroit Lions to force a one-game playoff, which Detroit won in a 31–27 comeback victory.
St. Clair once again started at least ten games in each of the 1958–1961 seasons, receiving Pro Bowl honors each year. He missed time due to an Achilles injury in 1962, but returned to play the entire 1963 season, for which he received the 49ers' Len Eshmont Award. During the 1964 preseason, he injured his other Achilles tendon during punt return practice, requiring career-ending surgery.
A perennial team captain, St. Clair was nicknamed "The Geek" by his teammates due to his eccentric off-the-field behavior, including a habit of eating raw meat, which he frequently used to intimidate 49ers rookies.
St. Clair was elected to the Pro Football Hall of Fame in 1990. On January 19, 2001, the city of San Francisco renamed the field at Kezar Stadium in his honor in recognition of the 189 home games he played there, and his number was retired by the 49ers later that year.
While still an active player, St. Clair was elected to Daly City's city council in 1958, which included a term as mayor from 1961 to 1962; one of his mayoral and council colleagues was his high school coach Joe Verducci. The 49ers made arrangements for him to fly back to Daly City for council business during road trips. He was the county supervisor for San Mateo County from 1966 to 1974. For many years he owned a liquor store at 24th and Sanchez in Noe Valley, which still bears his name.
St. Clair broke his hip in February 2015; complications led to his death in Santa Rosa, California, on April 20, 2015, at the age of 84.
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