He previously played for the Seattle Seahawks, Baltimore Ravens, Tampa Bay Buccaneers and was traded from the Cleveland Browns in May 2006 for former 49ers quarterback Ken Dorsey to be Alex Smith's mentor backup.

Dilfer attended Aptos High School in California, and upon graduation attended Fresno State. He is married to Cassandra Dilfer, a former Fresno State swimmer, and they have three daughters (Madeline, Victoria & Delaney) and a son, now deceased (Trevin).

On April 27, 2003, the Dilfers lost their son, Trevin Scott Dilfer, who died in a California hospital after a 40-day battle with heart disease at the age of 5. On June 2, 2003 Trent made his first public comments regarding his family's loss, and still grieving, openly wept.

Dilfer's professional football career began when he was drafted by the Tampa Bay Buccaneers with their 1st pick in the [[1994 draft (6th overall) after his junior season at Fresno State. 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 dollar bonus due in March. He 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, Banks was replaced 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. Dilfer did the I'm Going to Disney World! commercial since game MVP Ray Lewis was seen as too controversial.

Surprisingly, Dilfer was released after the season. He was seen as a "caretaker" quarterback, due 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, which was viewed as a horrible mistake on the part of the Ravens and was highly criticized by both fans and the Baltimore press. In 2001 Grbac's passer rating was 5.5 points lower than Dilfer's was in 2000.