Druckenmiller was drafted in the first round (26th overall) of the 1997 NFL Draft by the San Francisco 49ers, who intended to groom him as Steve Young's successor; after the draft, 49ers coach Steve Mariucci commented about Druckenmiller: "I would like to think he's our quarterback of the future." Because Young had a hand injury, Mariucci decided to start Druckenmiller for the Week 2 game (September 7, 1997) against the St. Louis Rams. Although the 49ers won 15-12, Druckenmiller completed only 10 of his 27 attempted passes for 102 yards with one touchdown pass and three interceptions. In the fourth quarter, Druckenmiller was 0-for-5 with one interception and two near-interceptions.
Druckenmiller played in three more games: first in Week 3 backing up Steve Young in the 49ers' 33-7 win over the New Orleans Saints. In that game, Druckenmiller completed 4 of 6 pass attempts for 41 yards, was sacked once for 9 yards, and lost one yard on a rush attempt. The following week, the 49ers beat the Atlanta Falcons 34-7. Druckenmiller was 2-for-7 for 32 yards and a 6-yard sack, and -3 yards rushing. Druckenmiller's next game action would be in the 49ers' final 1997 regular season game, a 38-9 loss to the Seattle Seahawks in which Druckenmiller was 5-for-11 for 64 yards, one interception, one sack, and one rushing yard. He finished the 1997 season 21-for-52 with one touchdown pass and four interceptions.
In the 1998 season, Druckenmiller played only two games: Week 2 against the Washington Redskins and Week 6 against the New Orleans Saints.
On September 6, 1999, the 49ers traded Druckenmiller to the Miami Dolphins for a conditional draft choice. Druckenmiller never played any games in 1999. In a preseason game on August 9, 2000, Druckenmiller completed 13 of 21 pass attempts in the Dolphins' 13-10 loss to the Pittsburgh Steelers for 141 yards including the 78-yard first touchdown drive. The Dolphins cut Druckenmiller on August 16.
He also played for the Memphis Maniax of the XFL in 2001. He ranked 13th in the league in rushing yards (208, leading all quarterbacks) and fourth in passer rating, with 13 touchdowns and seven interceptions.