To be clear, chrome://net-internals/#dns always shows the correct list when I check; there appear to be resolvers not present in that list.

resolver1.level3.net?  Any idea where we'd get that from?

We will talk to Google DNS when we see a DNS error, to check if your DNS seems to be working and you have an internet connection, I assume that's not what you're seeing?  (We won't send the DNS address you were looking up to GDNS - we just look up google.com or somesuch).

Adding 'Needs-Milestone' label, TE will check the issue and update the bug with comments & tag with respective Mstone

This is the tcpdump of me accessing https://jenkins.lucidchart.com in this state after clearing the host cache.

(Resources are loaded from aarjithn.github.io and fonts.googleapis.com; must be doing some prefetch for those.)

$ sudo tcpdump -i any udp
tcpdump: verbose output suppressed, use -v or -vv for full protocol decode
listening on any, link-type LINUX_SLL (Linux cooked), capture size 65535 bytes
10:49:50.753165 IP6 ip6-localhost.49882 > ip6-localhost.50047: UDP, length 0
10:49:52.131408 IP 192.168.0.1.50743 > 255.255.255.255.7437: UDP, length 173
10:49:52.261267 IP paul.office.lucidchart.com.58018 > resolver1.level3.net.domain: 29369+ A? jenkins.lucidchart.com. (40)
10:49:52.261564 IP paul.office.lucidchart.com.44644 > resolver1.level3.net.domain: 6304+ A? aarjithn.github.io. (36)
10:49:52.261870 IP paul.office.lucidchart.com.17899 > resolver1.level3.net.domain: 52157+ A? fonts.googleapis.com. (38)
10:49:52.286286 IP resolver1.level3.net.domain > paul.office.lucidchart.com.17899: 52157 2/0/0 CNAME googleadapis.l.google.com., A 216.58.203.42 (90)
10:49:52.463002 IP resolver1.level3.net.domain > paul.office.lucidchart.com.44644: 6304 2/0/0 CNAME github.map.fastly.net., A 151.101.24.133 (87)
10:49:52.478081 IP resolver1.level3.net.domain > paul.office.lucidchart.com.58018: 29369 NXDomain 0/1/0 (118)
10:49:52.478358 IP paul.office.lucidchart.com.54168 > resolver1.level3.net.domain: 34931+ A? jenkins.lucidchart.com.office.lucidchart.com. (62)
10:49:52.501567 IP resolver1.level3.net.domain > paul.office.lucidchart.com.54168: 34931 2/0/0 CNAME office.lucidchart.com., A 65.181.56.178 (92)

Maybe unrelated, but if anyone knows how I can prevent the DNS suffix search, that would also help me.

(DNS suffix search being the part where it goes from trying jenkins.lucidchart.com to jenkins.lucidchart.com.office.lucidchart.com because my local hostname is paul.office.lucidchart.com.)

Err....sorry 209.244.0.3 is resolver1.level3.net (didn't have a reverse DNS entry).

It does seem that Chrome is pretty aggressive about marking DNS servers as down and keeping them as down...but the issue can be resolved.

I filed a separate bug with the suffix search problems I'm having https://bugs.chromium.org/p/chromium/issues/detail?id=676085

Once a server fails for a particular number of attempts in a row (I think we get the number of attempts from the local DNS configuration), I don't believe we'll ever try it again as long as we have another (Another two?) servers that have not failed that number of times in a row, unless we reload the DNS configuration (And perhaps only if the DNS configuration has changed from when we last read it).