Once Seattle is awarded a franchise and gets in at number 32, the league will remain at that number for a long time. But theoretically, there are many areas with enough population that could accept a team if they had a team and a decent owner.
Let's say the league is healthy in 2035 and announces a four-team expansion to Houston, Quebec City, A Second Toronto/Hamilton franchise, and Portland. You'd have 36 teams, divided into six divisions of six.
MTL, OTT, QUE, BOS, TOR, TOR 2
BUF, NYI, NYR, NJ, WSH, PHI
DET, PIT, CBJ, CAR, FLA, TB
CGY, EDM, VAN, WPG, SEA, POR
NSH, CHI, STL, MIN, DAL, HOU
LV, ARI, SJ, LA, ANA, COL
2050 rolls around and Kansas City, San Francisco, Atlanta 3.0, and Austin would make for a 40 team league. You could have an NFL-like alignment of four-team divisions.
TOR, TOR 2, DET, BUF
MTL, OTT, QUE, BOS
NYI, NYR, NJ, WSH
PHI, PIT, CBJ, CAR
NSH, ATL, FLA, TB
CHI, STL, KC, MIN
DAL, HOU, AUS, COL
CGY, EDM, WPG, VAN
SEA, POR, LV, ARI
SJ, SF, LA, ANA
So, 32 is were we are likely going to stay for a while, 36 would be fine, and 40 would be the absolute most.