Despite all the information on Caravanistan and the web about the Caspian Sea crossings from Baku, it was still a bit of a hassle and adventure for me due to my late Azeri and therefore late Turkmen visa. I did however learn a fair bit. It seems to me that it can be troublesome because in Baku there is no central coordinator, everyone involved only knows a bit about their little world, the ferry schedules etc. This is what I can put together, hopefully I am not making it too easy and less interesting for everyone:
There are 4 places to buy tickets, they seem to change only because of the erratic work hours.
1. Ticket "office" SW of New City Park, maybe what has been referred to as ticket office of the Old Ferry port. More or less the one shown on page 209 of the Georgia... Azer Lonely Planet 2012 (the train rails are gone and ferry dock is further west). There is a steel gate and a trailer office, with guards and some ladies hanging around who know something about tickets. If there is a ferry at this port, they may sell you a ticket otherwise they will ask you to call the now well known phone numbers or go to the port near Nagila Cafe.
2. Official ticket office of old ferry port (Gps 40.372931, 49.861316). This is where you are directed if you ask at the big "Passenger Terminal" building at the east end of the Bulvar. From the sea side of the terminal building, go east along the new concreted drive/walkway a few hundred metres, look for a gate on the right through the white construction site boarding. It is actually a continuation of the road from kassa 1, so there should be another gate on your left. This looks like a proper office with a board listing prices ($90 Turkmenbashi, $110 Aktau... says including cabin and meals if available), ask guards for opening times. They sell tickets for Azeri ferries only and maybe only ones for this port.
3. Kassa in Ro Ro ferry port, 7km east of old ferry port (Gps 40.362907, 49.934454). Near Nagila cafe. Bus 46 goes from 28 May metro along Nobel Prospekti, then abruptly turns left at Nagila cafe (looks closed but still a landmark), the way to the kassa is a few hundred metres back, and is well described on Caravanistan's ferry page. Sounds like this is the "main" kassa where you can buy the Alat ferry tickets (to Turkmenbashi or Aktau), it was however closed the 2 times I went so better phone first.
4. Onboard the Turkmenistan flagged ferry (currently only the Berkarar) from the passenger manager. About $50 seat, $105 single, $160 twin.
First and hardest part is the ferry schedule and which kassa to go to. The ticket offices and ports are fairly well identified now.
1. Phone the numbers listed in Caravanistan's Caspian Sea article, they will tell you what to do.
2. If you see a ferry docked at the old port or know one is arriving, check at the 2 old ferry port kassas. This seems to be only for Turkmenbashi bound Azeri ferries.
3. For the Turkmen ferry, check http://www.marinetraffic.com
then ask around the old ferry port for a more "precise" time once you know it is approaching. The Turkmen passengers phone someone to ask but I don't know the number, some of their timing was as bad as mine (12 to 30 hours too early). Note the Azeri immigration don't like people boarding in the middle of the night, so come during normal hours if possible.
Second part is boarding, from my week and half observations in June only 2 ports are useful for travellers (Ro Ro port perhaps also for Alat ferries but kassas tell everyone to go to Alat?!):
1. Old ferry port, has only one dock, visible from the Baku waterfront. Get here via ticket office 2, cars maybe through another gate. Azeri ferry Bestekar Gara Garayev was going back and forth continuously, Turkmen Berkarar about once a week. Both to Turkmenbashi. No other ferries so every other day sounds about right.
2. Alat port. Turkmenbashi and Aktau bound ferries. Bus 20 starting from 28 May metro, then where it ends on roundabout near aquatic center end of city, change to 195 (Qobustan, Alat).
From marinetraffic and chatter around the kassas, seems like more ferries here but I think longer, roundabout sea route and less convenient for backpackers. Alat is at the end of a major cross country highway and rail line, so makes sense for cargo.
In the end skipped the Alat option and went the Berkarar route as it seemed faster (visa running out), easier and new so more interesting. Gara Garayev had very fast turn around the day before so I missed it as I didn't have Turkmen visa yet.
Azeri immigration insist on seeing the actual Turkmen visa to board, if only official LOI is enough it would so much easier.
Third part, just lots of waiting (0.5 to 1.5 days) for boat to go then to dock.
Fourth part: Departing at Turkmenbashi. Ferry docks very near train station but immigration office is nearly 2km east. If you can clear customs fast (seems tourists go after locals but before those with vehicles), there may be a bus, otherwise you need to either walk to town or get a taxi (phone or from highway). No facilities other than waiting room here but taxis accept usd. For those with vehicles or visa issues more waiting.
What happens if your Turkmen transit visa is about to run out?
1. They don't notice or are in a good mood, you are allowed in then go as fast as you can. They told me one day late is OK (At first I had less than 12 hours to go from Turkmenbashi to Dashogus without own vehicle, Hojeli border was closed. Even with own vehicle probably still no chance after waiting to clear vehicle). I presume at other side of country, you'll get ejected there so all good, just lay low on the way.
2. It is early on a weekday, Ashgabat central immigration ministry is working and they are in a good mood. They offer you a visa extension (3 to 5 days) where you write a letter to the head of the relevant ministry requesting an "exit visa" of a few more days. If it is accepted you pay for visa again ($55) and are cleared to carry on. From a blog it seems this may also happen if your visa has run out before entry.
BTW Ashgabat Northern "bus station" mentioned in LP is now open. It is a few km north of city, and known as awtomenzil. So don't be surprised if your shared taxi drops you here. May also be 2, quiet one for big bus and one for taxis/minibus.