Miller was projected to be a first round pick; however, his slightly disappointing performance at the combine caused him to be drafted early in the second round (38th overall), by the Oakland Raiders. Miller's successful college career drew high hopes for the Raider Nation. He was expected to be a reliable receiving threat and a solid blocker for the Raiders, after many disappointments at the team's tight end position, including Doug Jolley, Courtney Anderson and Randal Williams, and he fulfilled those expectations. Miller's blocking was a large factor in the Raiders' running game. He finished his rookie year with 44 catches for 444 yards and 3 touchdowns. Miller was added to the AFC 2011 Pro Bowl roster after Antonio Gates withdrew due to injury. Miller led the Raiders in receiving in 2008, 2009, and 2010, totaling 60 receptions for 685 yards and a career-high five touchdowns during the 2010 campaign. His receptions total was the eighth-highest among NFL tight ends. Miller moved into third place on the Raiders career receiving list for tight ends with 226 receptions over four seasons. His career totals during his time with Oakland include 2,712 receiving yards and 12 touchdowns.
On August 2, 2011, Miller signed with the Seattle Seahawks on a 5 year, $34 million deal, $17 million of which is guaranteed. Head Coach Pete Carroll stated that Miller would become a great part of the offense. He finished off his first season with 25 receptions for 233 yards and no touchdowns catches. Miller was played more as a blocking tight end during the season.