(Click to enlarge)

The word media appeared under the title for a while, clicking the title or anywhere in that block does nothing.

Can you be more specific what the "gallery block" is. It could be main_multi_content, main_gallery_embed, main_content, or main_image_fader.

main_image_fader, it does eventually load the image, but the initial view is as on screenshot.

The issue was a bit complex. The block doesn't by default fit in a column, but we have a bit of Tempcode on the default page setting a flag to make it choose a different layout. With caching, the flag didn't carry through.

I will fix via passing in a formal block_id parameter instead. This will require editing the Comcode to include:
block_id="small_version"