Howton played college football at Rice Institute in Houston,[5] where he was nicknamed "Red Fox" not only for his hair color, but also for the way he ran pass patterns, which made him a great offensive end, establishing a season record for average yards (22.6) on pass receptions.

At the 1948 track and field regional meet in Lubbock, he had a time of 14.3 in the high hurdle event, setting a record that stood for several decades.

In 1951, he finished his college football career with 64 catches for 1,289 yards and 12 touchdowns, on his way to earn the following honors: In 1971, he was inducted into the Rice Athletic Hall of Fame.

As a rookie, he earned immediate comparisons with Hall of Famer Don Hutson, with his speed, sure hands, and big-play ability.

In January 1959, the Packers hired Vince Lombardi as head coach and general manager after the team's worst record ever (1–10–1) in 1958.

In April, Lombardi traded Howton to the Cleveland Browns in exchange for defensive end Bill Quinlan and halfback Lew Carpenter.

[11] Howton played only one season in Cleveland, leading the team in receptions with 39, and experiencing what would be the only winning campaign of his NFL career.

The expansion Dallas Cowboys convinced him to play in his home state and traded a draft choice to the Browns in exchange for his rights.

That season the Cowboys recorded only a tie, which came against the New York Giants at Yankee Stadium on December 4, when a late touchdown pass from Eddie LeBaron to Howton finalized a 31–31 comeback, against a team that had made championship game appearances in three of the previous four years.

[12] The first win in franchise history came during the 1961 season opener against the Pittsburgh Steelers, 27–24, with Howton contributing a game-high 138 receiving yards and a touchdown.

Howton was also the top receiver from those players in the 1952 NFL draft, which included future Hall of Famers such as Frank Gifford, Ollie Matson, and Hugh McElhenny.