The Pacific Northwest derby is unique in having a history dating back to the days of the old North American Soccer League (NASL) in the 1970s.
But, while always a special date in the diary for fans, this year's clash has been given extra spice by Dempsey's high-profile return to MLS from the Premier League.
Dempsey was a surprise arrival earlier this month when the Sounders signed him on a $5 million per year deal after he fell down the pecking order at Tottenham Hotspur, just one year after joining them from London neighbours Fulham.
The Texans is, along with Landon Donovan, the best known American player and was expected to stay in the Premier League for several more years but was tempted home early, being unveiled on the pitch to delighted fans before a game with Dallas.
"That was incredible. That was like a movie. I can't even imagine what it's going to be like when the whole stadium is completely packed and they're behind us," said Dempsey.
"We'll feed off that energy and we'll make sure we give everything we have to let them go home happy."
The 30-year-old made his Sounders debut at Toronto on Aug. 10 and featured last week in Houston but Sunday's sell-out will be his first opportunity to play in front of his home fans and Dempsey knows a local derby means expectations will be high.
"It's big. The fans are really going to be up for it as you can see - 67,000-68,000 fans coming out to the game," he said.
"I'm used to the derbies and used to the rivalries and I understand the importance of it. Hopefully I can open my account this weekend against them."
"It's bragging rights. It's going to be an intense game, people are going to fight to the end. You know how much it means to the fans and making sure they go home happy. We're going to do everything we can to make sure that happens," he added.
While the Sounders, who also feature Nigeria's former Inter Milan and Newcastle United forward Obafemi Martins, are MLS's biggest success story in terms of crowds, averaging over 40,000 per game, the Timbers are having a better time on the field.
Portland are third in the Western Conference while the Sounders are down in seventh outside the playoff positions.
But Sunday's clash is about much more than three points for supporters who remember the meetings in the lower tier USL league in the days before the two teams were moved up to MLS.
"It's really every bit the rivalry that people overseas in the big derby cities are used to seeing," Timbers president Merritt Paulson told Reuters.
"There is nothing fabricated about this. There is over 40 years of history behind it and you need that history to have an authentic rivalry.
"The cities are close enough that it has the proximity factor and there is a natural rivalry extending beyond soccer between Seattle and Portland.
"Plus we have the two biggest fan bases and certainly the most passionate fan bases in soccer in North America," he added.
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