John Constantine Unitas was born in Pittsburgh in 1933 to Francis J. Unitas and Helen Superfisky, who both were of Lithuanian descent; he grew up in the Mount Washington neighborhood. When Johnny was five years old, his father died of cardiovascular renal disease complicated by pneumonia, leaving the young boy to be raised by his mother, who worked two jobs to support the family. His surname was a result of a phonetic transliteration of a common Lithuanian last name Jonaitis. Attending St. Justin's High School in Pittsburgh, Unitas played halfback and quarterback.

The 1964 season would see the Colts return to the top of the Western Conference. After dropping their season opener to the Minnesota Vikings, the Colts ran off 10 straight victories to finish with a 12-2 record. The season was one of Unitas' best as he finished with 2,824 yards passing, a league-best 9.26 yards per pass attempt, 19 touchdown passes and only 6 interceptions. He was named the NFL's Most Valuable Player by the AP and UPI for a second time. However, the season would end on a disappointing note for the Colts as they were upset by the Cleveland Browns in the 1964 NFL Championship Game, losing 27-0. Unitas resumed his torrid passing in 1965, as he threw for 2,530 yards, 23 touchdowns and finished with a league-high and career best 97.1 passer rating. But he was lost for the balance of the season due to a knee injury in a week 12 loss to the Bears. More postseason heartbreak would follow in 1965. The Colts and Packers finished in a tie for first place in the Western Conference and a one-game playoff was played in Green Bay to decide who would be the conference representative in the 1965 NFL Championship Game. The Colts lost in overtime 13-10 due in large part to a game-tying field goal by Don Chandler that many say was incorrectly ruled good. Backup quarterback Gary Cuozzo also suffered a season-ending injury the following week and it would be running back Tom Matte who filled in as the emergency QB for the regular-season finale and the playoff loss to the Packers. Unitas, healthy once more, threw for 2748 yards and 22 touchdowns in 1966 in a return to Pro Bowl form. However, he posted a league-high 24 interceptions.

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