It turns out that this ancient bug can be reproduced by causing a block to error and slotting it inside another.
Hm, seems like the error halo is impacting how the width of the block is being calculated. The same issue occurs with currently running blocks.
The other time I’ve encountered this bug is when the page seems to run out of resources and turn entirely white. Then moving the mouse around/changing the page zoom can fix the page, but sometimes some of the blocks will become way too long.