Hi Stephen,
Comparing the HTML using Firefox/Firebug, I see both good and bad pages have the correct HTML to display the "Edit columns" heading. However the bad page has missing CSS styling.
On Fedora rawhide, with an up to date "locate" database, I can see an empty CSS file that looks suspicious.
$ ls -l `locate datagrid | grep css`
-rw-r--r--. 1 root root 6251 May 27 15:03 /usr/lib/python2.7/site-packages/djblets/htdocs/static/djblets/css/datagrid.css
-rw-r--r--. 1 root root 6316 May 27 15:03 /usr/lib/python2.7/site-packages/djblets/htdocs/static/djblets/css/datagrid.da6c340af879.css
-rw-r--r--. 1 root root 6316 May 27 02:01 /usr/lib/python2.7/site-packages/djblets/htdocs/static/djblets/css/datagrid.min.6521a0d8b348.css
-rw-r--r--. 1 root root 0 May 27 15:03 /usr/lib/python2.7/site-packages/djblets/htdocs/static/djblets/css/datagrid.min.css
-rw-r--r--. 1 root root 0 May 27 15:03 /usr/lib/python2.7/site-packages/djblets/htdocs/static/djblets/css/datagrid.min.d41d8cd98f00.css
-rw-r--r--. 1 root root 6251 May 27 02:01 /usr/lib/python2.7/site-packages/djblets/static/djblets/css/datagrid.css
I expect those two empty files are (part of) the problem.