With Dempsey's first two appearances for Seattle coming on the road, fans flocked to CenturyLink Field to witness the American international's first home match as a Sounder - the attendance figure of 67,385 was the second largest stand-alone crowd in MLS history.
But the spectators saw Johnson nab the only goal of the game as his strike in the 60th minute proved to be the difference between the two rivals.
Portland had the better run of play in the opening period, which culminated in the 35th minute with Diego Valeri's right-footed shot hitting the post.
The two sides remained scoreless until the hour mark when the Sounders were awarded a free kick near the sideline.
Johnson drew the foul and ultimately made the most of the restart as his glancing header from a Mauro Rosales delivery ended up in the back of the net.
Seattle created a number of scoring opportunities in the final stages but failed to extend its lead, instead settling for a one-goal victory that lifts the club to 37 points on the season.
Portland, suffering just its fourth loss of the season, has claimed just one league win from its last six contests. The Timbers exit the weekend in fourth place in the Western Conference with 39 points.
08/26 00:18:51 ET