SSH uses public-key cryptography to authenticate the remote computer and allow it to authenticate the user, if necessary. There are several ways to use SSH; one is to use automatically generated public-private key pairs to simply encrypt a network connection, and then use password authentication to log on.

Another is to use a manually generated public-private key pair to perform the authentication, allowing users or programs to log in without having to specify a password. In this scenario, anyone can produce a matching pair of different keys (public and private). The public key is placed on all computers that must allow access to the owner of the matching private key (the owner keeps the private key secret). While authentication is based on the private key, the key itself is never transferred through the network during authentication. SSH only verifies whether the same person offering the public key also owns the matching private key. In all versions of SSH it is important to verify unknown public keys, i.e. associate the public keys with identities, before accepting them as valid. Accepting an attacker's public key without validation will authorize an unauthorized attacker as a valid user

On Unix-like systems, the list of authorized public keys is typically stored in the home directory of the user that is allowed to log in remotely, in the file ~/.ssh/authorized_keys. This file is respected by SSH only if it is not writable by anything apart from the owner and root. When the public key is present on the remote end and the matching private key is present on the local end, typing in the password is no longer required (some software like Message Passing Interface (MPI) stack may need this password-less access to run properly). However, for additional security the private key itself can be locked with a passphrase.

The private key can also be looked for in standard places, and its full path can be specified as a command line setting (the option -i for ssh). The ssh-keygen utility produces the public and private keys, always in pairs.

SSH also supports password-based authentication that is encrypted by automatically generated keys. In this case, the attacker could imitate the legitimate server side, ask for the password, and obtain it (man-in-the-middle attack). However, this is possible only if the two sides have never authenticated before, as SSH remembers the key that the server side previously used. The SSH client raises a warning before accepting the key of a new, previously unknown server. Password authentication can be disabled.

SSH is typically used to log into a remote machine and execute commands, but it also supports tunneling, forwarding TCP ports and X11 connections; it can transfer files using the associated SSH file transfer (SFTP) or secure copy (SCP) protocols. SSH uses the client-server model.

The standard TCP port 22 has been assigned for contacting SSH servers.

An SSH client program is typically used for establishing connections to an SSH daemon accepting remote connections. Both are commonly present on most modern operating systems, including macOS, most distributions of Linux, OpenBSD, FreeBSD, NetBSD, Solaris and OpenVMS. Notably, versions of Windows prior to 1709 do not include SSH by default. Proprietary, freeware and open source (e.g. PuTTY, and the version of OpenSSH which is part of Cygwin) versions of various levels of complexity and completeness exist. File managers for UNIX-like systems (e.g. Konqueror) can use the FISH protocol to provide a split-pane GUI with drag-and-drop. The open source Windows program WinSCP provides similar file management (synchronization, copy, remote delete) capability using PuTTY as a back-end. Both WinSCP and PuTTY are available packaged to run directly off a USB drive, without requiring installation on the client machine. Setting up an SSH server in Windows typically involves enabling a feature in Settings app. In Windows 10 version 1709, an official Win32 port of OpenSSH is available.

SSH is important in cloud computing to solve connectivity problems, avoiding the security issues of exposing a cloud-based virtual machine directly on the Internet. An SSH tunnel can provide a secure path over the Internet, through a firewall to a virtual machine.

SSH is a protocol that can be used for many applications across many platforms including most Unix variants (Linux, the BSDs including Apple's macOS, and Solaris), as well as Microsoft Windows. Some of the applications below may require features that are only available or compatible with specific SSH clients or servers. For example, using the SSH protocol to implement a VPN is possible, but presently only with the OpenSSH server and client implementation.

- For login to a shell on a remote host (replacing Telnet and rlogin)

- For executing a single command on a remote host (replacing rsh)

- For setting up automatic (passwordless) login to a remote server (for example, using OpenSSH)

- In combination with rsync to back up, copy and mirror files efficiently and securely

- For forwarding or tunneling a port (not to be confused with a VPN, which routes packets between different networks, or bridges two broadcast domains into one).

- For using as a full-fledged encrypted VPN. Note that only OpenSSH server and client supports this feature.

- For forwarding X from a remote host (possible through multiple intermediate hosts)

- For browsing the web through an encrypted proxy connection with SSH clients that support the SOCKS protocol.

- For securely mounting a directory on a remote server as a filesystem on a local computer using SSHFS.

- For automated remote monitoring and management of servers through one or more of the mechanisms discussed above.

- For development on a mobile or embedded device that supports SSH.

- For securing file transfer protocols.