Dilfer attended Aptos High School in California.

Dilfer attended Fresno State. As a starter for 2 1⁄2 seasons for the Bulldogs, Dilfer helped Fresno State win or share the conference title for three straight seasons and started in two bowl games. In his junior season, Dilfer led the nation in pass efficiency en route to being named the WAC Offensive Player of the Year. He also set the NCAA record for consecutive pass attempts without an interception (271) that would stand until 2007, when Kentucky quarterback Andre' Woodson broke it. He would then forgo his senior season to declare himself eligible for the 1994 NFL Draft.

Dilfer's professional football career began when he was drafted by the Tampa Bay Buccaneers with their 1st pick in the 1994 NFL Draft (6th overall) after his junior season at Fresno State.

Enlisted as the starter in his second year, after seeing spot duty in his rookie year, Dilfer struggled during what was still a dark period for the Buccaneers as a whole, when in 1995 he threw only 4 TD passes but 18 interceptions. The following year, he showed moderate improvement by upping his TD production, but failed to improve his turnover numbers (recording a career-high 19).

The following season, a year that Tampa's offense was aided by the arrival of rookie Warrick Dunn and the emergence of Mike Alstott, Dilfer was the first Tampa Bay quarterback to ever go to the Pro Bowl, which some say was a reward for a highly efficient season in the Buccaneers' limited offense. In the first 12 games of that year Dilfer passed for 2213 yards, 19 touchdowns and five interceptions. However, Dilfer's performance was perceived to decline in his last four games. In the playoffs the Buccaneers defeated their NFC Central rivals, the Detroit Lions, before losing to their long-time division rivals, and defending Super Bowl champions, the Green Bay Packers. While with the Bucs, he won more games than any quarterback in franchise history and took the team to their first playoff game in 15 years.

Dilfer threw for 21 touchdowns with the Tampa Bay Buccaneers in both the 1997 and the 1998 NFL seasons. In the 1996-1999 NFL seasons, with the Tampa Bay Buccaneers, Dilfer averaged 2,729 yards a season and had a total of 58 touchdowns.

After the 1999 season, the Bucs granted unconditional free-agent status to Dilfer on 11 February 2000, rather than pay him a $4.6 million bonus due in March. Also compounding matters was the collarbone injury suffered by Dilfer midseason in 1999 and the subsequent winning streak that coincided with the insertion of QB Shaun King into the lineup, with the Bucs going to the NFC Championship Game that season, and making Dilfer expendable.

Dilfer signed with the Ravens on March 8, 2000 and became the backup for Tony Banks. After two straight losses and four straight weeks without an offensive touchdown, the Ravens replaced Banks with Dilfer. The Ravens would lose their third straight game and fail to score a touchdown for the fifth straight week. It would be the last time the Ravens would lose that season, or go without a touchdown. The Ravens finished the season winning seven straight to earn a wild card berth at 12-4. The 7-1 run also gave Dilfer a 45-39 record as a starter at that point.

In the playoffs, Dilfer went 3-0, and the Ravens advanced to Super Bowl XXXV in Tampa to meet the New York Giants. Halfway through the first quarter Dilfer connected with Brandon Stokley on a deep post for a 38-yard touchdown, badly beating Jason Sehorn. A third down 44-yard pass to Qadry Ismail would set up a field goal before halftime, to give Baltimore a 10-0 lead. The Ravens eventually won easily, 34-7. Dilfer's game stats were 12 completions for 153 yards and 1 TD.

Not surprisingly, the Super Bowl win and the fans' disenchantment with previous starter Tony Banks combined to make Dilfer hugely popular in Baltimore. It was, then, much to their and his surprise and chagrin that management elected to release Dilfer at season's end, making him the first and only Super Bowl winning quarterback ever released the following year. Dilfer was seen as a "caretaker" quarterback by the organization: his success attributed entirely to the strength of the Ravens' defense and head coach Brian Billick's run-heavy offense. He was replaced by Kansas City Chiefs' Pro Bowler Elvis Grbac, a somewhat controversial decision. In 2001 Grbac's passer rating was 5.5 points lower than Dilfer's was in 2000.