Tolliver was slated to compete with Tommy Maddox for the backup quarterback spot at Atlanta as training camp rolled around. Halfway through August, Maddox was released, and Tolliver was made the primary backup behind Chris Chandler. Tolliver played his first NFL game since 1994 on September 7, 1997 against the Carolina Panthers. He completed 7 of 17 passes for 79 yards. After relieving Chandler again the following week, Tolliver was slated to start the next game against the 49ers, in what became his only starting appearance of the season. He was slated to start again against the Denver Broncos, but instead came in late in the game. He was almost able to lead the Falcons to a comeback victory over the Broncos, completing six of nine passes for 85 yards and a touchdown, but he instead lost to the then-undefeated Broncos as the team remained winless. When Chandler went down with an injury in late October, coach Dan Reeves chose to start Tony Graziani. Shortly afterwards, Tolliver was released by the Falcons. In early November, Kansas City Chiefs quarterback Elvis Grbac was lost for the season due to a broken collarbone. As a result, the Chiefs signed Tolliver to a two-year contract as the third-string quarterback to replace him. Tolliver finished the season having completed 64 passes in 116 attempts for 677 yards, five touchdowns, and one interception. Only one of the 116 attempts came as a Kansas City quarterback. The 1998 preseason began with Tolliver competing with Pat Barnes for the third-string quarterback job, but this ended when Tolliver was released by the Chiefs in August.