It was Vancouver's third consecutive defeat, and sixth straight on the road.
"A disappointing result for us, and also a disappointing performance. I don't think we played anywhere near our best today," said Whitecaps manager Martin Rennie. "This wasn't anywhere near the standard we would expect from anybody and we have to turn it around."
Vancouver (10-10-7) finished the match with 10 men after striker Darron Mattocks earned a straight red card for an elbow to the head of Portland defender David Horst in the 84th minute.
Portland (6-13-6) had not won since a 2-1 victory over San Jose on July 3.
The Whitecaps saw the return of captain Jay DeMerit, who sustained a concussion in Vancouver's win over Real Salt Lake on Aug. 11. Midfielder Barry Robson also returned after a one-game suspension for behaviour toward an assistant referee in a loss to Dallas two weekends ago.
In the first half, Miller's 45th-minute equalizer concluded an opening frame where the Whitecaps were under near constant pressure from their hosts. Having controlled tempo and possession in the game's earliest moments, the visitors were pushed back into their own half for the remainder of the period.
Portland forward Franck Songo'o was a nuisance throughout, peppering goalkeeper Joe Cannon with shots and crosses. Yet it was a simple build-up through the middle that saw the Timbers tally first.
Darlington Nagbe scored in his third consecutive match, easily slipping through the Vancouver defence and slotting a shot past Cannon in the 41st minute.
The lead was short-lived, however, as DeMerit emerged from a goalmouth scramble in the half's waning moments, lacing a diagonal pass to a wide-open Miller. The Scottish striker beat Donovan Ricketts to the near post, levelling the score and seemingly giving Vancouver new life.
Instead Portland retook the lead in the 55th minute when Songo'o, who had been so dangerous from the run of play in the first half, swerved a free kick under a diving Cannon at the near post.
"I probably was a bit too casual on it. I don't know if I took my eye off it or my grip wasn't good," Cannon said.
Vancouver's best chance of the second half came in the 74th minute as Camilo lured Ricketts out of goal on the left, but Steven Smith headed the Brazilian's subsequent shot off the line. Two minutes later, Miller headed Y.P. Lee's cross just wide as the Whitecaps grew increasingly frustrated.
"We just didn't connect our passes and we didn't really threaten them too much in behind," Rennie explained. "When we did, we looked dangerous. But we didn't do that enough and we didn't make them defend enough."
The Whitecaps received a further setback when Mattocks, the hero of Vancouver's first game in Portland this season, was sent off despite having only entered the game as a 65th-minute substitute. That card was the eighth of the season for Mattocks and earns him another automatic suspension.
"It's an issue we've talked a lot to Darren about. I don't think he's ever malicious, I don't think there's any intent. But if he's challenging with his arm up, and he connects, that can happen," said Rennie.
The shorthanded Whitecaps could do little as the match crept toward completion, repeatedly giving the ball away in their haste to find a second equalizer.
Despite the string of losses, captain DeMerit remained optimistic.
"We're not in a dire situation right now. It's nothing that a good couple of performances can't turn around," the American said.