At least that tells me there's more to it than just a few frames maybe getting dropped when pausing.
The timestamps
Blue Iris provides with each H.264 frame only provide precision of about 0.36 seconds for a 1 hour clip (because the timestamps are integers from 0 to 10000, and 1 hour divided by 10000 is 0.36 seconds). So rounding error can't account for that much difference either.
Well it is a shame Blue Iris does not have a decent way to ingest someone else's clip for web server streaming because I might be able to figure something out with that one. Big errors like 20 seconds or 2 minutes are a lot easier to hunt down than tiny ones like a half second.
If you PM me login details for your server (It doesn't need to be an admin account, and you can limit me to just that one camera, that would be fine), I can log in and debug and try to play / snapshot that clip through UI3 myself and see if I can identify a problem. If this sounds like a good idea to you, then I suggest you flag and protect that clip so it doesn't get cleared out automatically.