My take is that there was a broad retreat from the tiny and often one-purpose worlds toward what are now the High Population worlds, while the medium population worlds (Pop 5-7) would have individual stories, and the High Pops all just carried on being big and multi-faceted. Much of this would have been settled in the first 300 years or so, but each region will have a different tale to tell.
"The Long Night" is a political term more than a cultural one; Imperial code for "when there wasn't an Empire of Man." I feel that some regions went pretty lonely and "dark" while others were regionally networked to the point that they barely noticed. The coreward part of the First and Second Imperia that we now know as Julian space is the most extreme of these. The regional banks in that area remained united, keeping the lights on, but the advent of the Vargr kept the area occupied enough that they were never able or inclined to reach very far to rimward into the rest of the old Imperium.
At the other end of the spectrum, I see much of the core become fractured and insular. While it rose centuries before becoming the Third Imperium, Sylea had to fight a surprising number of neighbors for primacy.
I think you'll see polities arise around the homes of the more successful Minor Races, both Human and Non-Human. Some were more driven than others, whether by racial pride (Geonee and Suerrat), necessity, or simple opportunism. These states will have risen and fallen, possibly more than once, during the Long Night, giving the enterprising Referee plenty of options to develop his particular subsectors and decades.
Then, of course, there is the Magyar and Daibei area, which was conquered in a rolling tide of clan ambitions by the Aslan. You want a persistent warzone either to play in or have nearby, the Aslan Conquest is often the best answer. Due to the clannishness of the Aslan, a Human campaign can make real gains against one Clan over the span of a campaign only to be lost to history when another Clan sees the opportunity and crushes the upstart Humans a generation later.
The areas beyond Imperial space also have a lot of potential. The rise and fall of the Darrians is during the Long Night. The farthest reach of the Zhodani, and the scourge of Vargr pirates across systems that must be taken "back" is during the Long Night. The stabilization of K'kree space, and the creation of the Hiver Federation are early in the Long Night, and much of the formative period in the entire Gateway region is around the same time.
With the understanding that you are unlikely to get the entire collection of Major Races in one place during this era, my advice is to pick a spot about the usual size for a healthy campaign (usually 2 to 4 subsectors) and decide what story you see there.