diff --git a/.github/.goss.yaml b/.github/.goss.yaml
index 6ccdf1851..e724f2aeb 100644
--- a/.github/.goss.yaml
+++ b/.github/.goss.yaml
@@ -13,20 +13,11 @@ file:
     group: wazuh-manager
     filetype: file
     contains: []
-  /var/wazuh-manager/etc/sslmanager.cert:
+  /var/wazuh-manager/etc/certs:
     exists: true
-    mode: "0644"
     owner: root
-    group: root
-    filetype: file
-    contains: []
-  /var/wazuh-manager/etc/sslmanager.key:
-    exists: true
-    mode: "0600"
-    owner: root
-    group: root
-    filetype: file
-    contains: []
+    group: wazuh-manager
+    filetype: directory
 user:
   wazuh-manager:
     exists: true
diff --git a/.github/workflows/5_check_integration_tools.yml b/.github/workflows/5_check_integration_tools.yml
index 9f7c60dad..e89af07db 100644
--- a/.github/workflows/5_check_integration_tools.yml
+++ b/.github/workflows/5_check_integration_tools.yml
@@ -597,7 +597,7 @@ jobs:
             set -e
             cd /tmp/wazuh-docker/${DEPLOYMENT}
             echo '=== Running certificate generation ==='
-            sudo bash /tmp/wazuh-docker/tools/utils/deployment/certificates-conf.sh --cert --copy
+            sudo bash /tmp/wazuh-docker/tools/utils/deployment/certificates-conf.sh --cert --copy --priv
             echo ''
             echo '=== Generated certificate files ==='
             find ./config -name '*.pem' | sort
@@ -675,6 +675,35 @@ jobs:
             exit 1
           "
 
+      - name: Verify manager certificates are unique per container
+        run: |
+          DEPLOYMENT="${{ matrix.deployment_type }}"
+          ssh ${{ env.SSH_OPTS }} "${{ env.REMOTE }}" "
+            set -eo pipefail
+            cd /tmp/wazuh-docker/${DEPLOYMENT}
+
+            rm -f /tmp/remoted-fingerprints.txt
+            for SVC in \$(sudo docker compose config --services | grep -E 'wazuh\.(manager|master|worker)'); do
+              echo \"=== \$SVC ===\"
+              sudo docker compose exec -T \$SVC ls -ld /var/wazuh-manager/etc/certs
+              sudo docker compose exec -T \$SVC ls -la /var/wazuh-manager/etc/certs
+              sudo docker compose exec -T \$SVC openssl x509 \
+                -in /var/wazuh-manager/etc/certs/remoted.pem -noout -subject -dates
+              sudo docker compose exec -T \$SVC openssl x509 \
+                -in /var/wazuh-manager/etc/certs/remoted.pem -noout -fingerprint \
+                | tee -a /tmp/remoted-fingerprints.txt
+            done
+
+            # Every manager node must hold its own self-signed certificate
+            DUPLICATED=\$(sort /tmp/remoted-fingerprints.txt | uniq -d)
+            if [ -n \"\$DUPLICATED\" ]; then
+              echo 'ERROR: the same remoted certificate is shared across manager nodes'
+              echo \"\$DUPLICATED\"
+              exit 1
+            fi
+            echo 'OK: each manager node has its own remoted certificate'
+          "
+
       - name: Cluster warm-up wait
         run: |
           if [ "${{ matrix.deployment_type }}" = "multi-node" ]; then
diff --git a/CHANGELOG.md b/CHANGELOG.md
index bb3f7f6b5..6264fbc12 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -10,6 +10,7 @@
 | Issue | Comment |
 | - | - |
 | [#2461](https://github.com/wazuh/wazuh-docker/issues/2461) | Added explicit `permissions` blocks to the 4.x workflows to restrict the `GITHUB_TOKEN` scope |
+| [#2601](https://github.com/wazuh/wazuh-docker/issues/2601) | Regenerate the manager self-signed server certificate per container at first boot |
 
 ### Removed
 
diff --git a/build-docker-images/wazuh-manager/Dockerfile b/build-docker-images/wazuh-manager/Dockerfile
index 91c6de341..1cd451ee0 100644
--- a/build-docker-images/wazuh-manager/Dockerfile
+++ b/build-docker-images/wazuh-manager/Dockerfile
@@ -45,8 +45,11 @@ RUN dnf install openssl findutils procps shadow-utils -y && \
     mkdir -p /var/wazuh-manager/etc/certs && \
     chown root:wazuh-manager /var/wazuh-manager/etc/certs && \
     chmod 1770 /var/wazuh-manager/etc/certs && \
-    rm -f /var/wazuh-manager/etc/sslmanager.key && \
-    rm -f /var/wazuh-manager/etc/sslmanager.cert
+    # Remove manager self-signed certificate/key
+    rm -f /var/wazuh-manager/etc/certs/remoted.pem \
+          /var/wazuh-manager/etc/certs/remoted-key.pem \
+          /var/wazuh-manager/etc/certs/apid.pem \
+          /var/wazuh-manager/etc/certs/apid-key.pem
 
 # Prepare permanent data snapshot (sync calls: https://github.com/docker/docker/issues/9547)
 RUN chmod 755 /permanent_data.sh && \
diff --git a/build-docker-images/wazuh-manager/config/etc/cont-init.d/0-wazuh-init b/build-docker-images/wazuh-manager/config/etc/cont-init.d/0-wazuh-init
index fa5010819..096e00fbd 100644
--- a/build-docker-images/wazuh-manager/config/etc/cont-init.d/0-wazuh-init
+++ b/build-docker-images/wazuh-manager/config/etc/cont-init.d/0-wazuh-init
@@ -44,6 +44,8 @@ mount_permanent_data() {
     # Check if the path is not empty
     if find ${permanent_dir} -mindepth 1 | read; then
       print "The path ${permanent_dir} is already mounted"
+    elif [ ! -d "${data_tmp}" ]; then
+      print "No permanent data snapshot for ${permanent_dir}, skipping"
     else
         print "Installing ${permanent_dir}"
         exec_cmd "cp -ar ${data_tmp}. ${permanent_dir}"
@@ -117,12 +119,93 @@ remove_data_files() {
 
 ##############################################################################
 # Create certificates: Manager
+#
+# The manager has a single self-signed server pair, etc/certs/remoted.*, read
+# both by remoted's HTTPS agent listener (<remote><https>) and by authd
+# (<auth><ssl_manager_cert>). The package post-install generates it, so the image
+# build removes it (see Dockerfile) and every container generates its own here:
+# no two containers from the same image share a private key.
+#
+# Both consumers are read from the configuration and generated independently, so
+# a deployment pointing one of them at a custom path still gets a valid pair.
+#
+# remoted opens these files after dropping privileges and does not start if they
+# are missing or unreadable, so this must run before the manager is started and
+# the files must end up wazuh-manager:wazuh-manager 0640.
 ##############################################################################
 
-create_wazuh_key_cert() {
-  print "Creating wazuh-authd key and cert"
-  exec_cmd "openssl genrsa -out ${WAZUH_INSTALL_PATH}/etc/sslmanager.key 4096"
-  exec_cmd "openssl req -new -x509 -key ${WAZUH_INSTALL_PATH}/etc/sslmanager.key -out ${WAZUH_INSTALL_PATH}/etc/sslmanager.cert -days 3650 -subj /CN=${HOSTNAME}/"
+# Certificate paths in the configuration are Wazuh-home relative, as the rest of
+# the manager configuration is.
+resolve_wazuh_path() {
+  case "$1" in
+    /*) echo "$1" ;;
+     *) echo "${WAZUH_INSTALL_PATH}/$1" ;;
+  esac
+}
+
+# $1: XML tag, $2: enclosing block
+get_conf_path() {
+  sed -n "/<$2>/,/<\/$2>/s|.*<$1>\(.*\)</$1>.*|\1|p" \
+    "${WAZUH_INSTALL_PATH}/etc/wazuh-manager.conf" | head -n1
+}
+
+# $1: certificate path, $2: key path
+create_server_cert_pair() {
+  local cert=$(resolve_wazuh_path "$1")
+  local key=$(resolve_wazuh_path "$2")
+
+  # Mixed-ownership directory: the daemons regenerate their own certificates here
+  # (group write), while the sticky bit keeps them from replacing the root-owned
+  # indexer trust material that shares the directory. Ownership and mode are
+  # best-effort: the directory may be a read-only mount, and failing to re-apply
+  # them must not stop the certificate from being created.
+  exec_cmd "mkdir -p $(dirname "${cert}") $(dirname "${key}")"
+  chown root:wazuh-manager "$(dirname "${cert}")" 2>/dev/null || true
+  chmod 1770 "$(dirname "${cert}")" 2>/dev/null || true
+
+  if [ -e "${cert}" ] && [ -e "${key}" ]
+  then
+    print "Manager server certificate ${cert} already present, skipping generation"
+  elif [ -e "${cert}" ] || [ -e "${key}" ]
+  then
+    # Same guard as the package post-install: never overwrite operator-provided
+    # material. Half a pair cannot be completed, so warn instead of guessing.
+    print "Warning: only one of ${cert} / ${key} is present; remoted will not start"
+    return
+  else
+    print "Creating the manager server certificate and key (${cert})"
+    ${WAZUH_INSTALL_PATH}/bin/wazuh-manager-remoted -C 3650 -B 4096 \
+      -S "/C=US/ST=California/CN=Wazuh/" -K "${key}" -X "${cert}" > /dev/null 2>&1 || \
+    exec_cmd "openssl req -x509 -newkey rsa:4096 -sha256 -days 3650 -nodes \
+      -keyout ${key} -out ${cert} -subj /C=US/ST=California/CN=Wazuh/"
+  fi
+
+  # remoted and authd read these after dropping privileges. Not fatal on failure:
+  # an operator-provided certificate may be a read-only bind mount.
+  chown wazuh-manager:wazuh-manager "${cert}" "${key}" 2>/dev/null || \
+    print "Warning: could not set ownership on ${cert} (read-only mount?)"
+  chmod 640 "${cert}" "${key}" 2>/dev/null || true
+}
+
+create_manager_server_certs() {
+  local https_cert=$(get_conf_path certificate https)
+  local https_key=$(get_conf_path key https)
+  local authd_cert=$(get_conf_path ssl_manager_cert auth)
+  local authd_key=$(get_conf_path ssl_manager_key auth)
+
+  # The manager has one self-signed pair and one identity: authd's
+  # <ssl_manager_cert> is derived from the HTTPS listener's <certificate> by the
+  # installation itself, and /enroll's mTLS mode treats that certificate as the
+  # enrollment credential. Only that pair is generated, exactly as the package
+  # post-install does; a mismatch can only come from hand-edited configuration.
+  create_server_cert_pair "${https_cert:-etc/certs/remoted.pem}" \
+                          "${https_key:-etc/certs/remoted-key.pem}"
+
+  if [ "${authd_cert:-etc/certs/remoted.pem}" != "${https_cert:-etc/certs/remoted.pem}" ] || \
+     [ "${authd_key:-etc/certs/remoted-key.pem}" != "${https_key:-etc/certs/remoted-key.pem}" ]
+  then
+    print "Warning: authd (${authd_cert}) and the HTTPS listener (${https_cert}) use different certificates; both must present the same manager identity"
+  fi
 }
 
 ##############################################################################
@@ -277,12 +360,6 @@ main() {
   # Remove some files in permanent_data (i.e. .template.db)
   remove_data_files
 
-  # Create wazuh-authd key and cert if not present
-  if [ ! -e ${WAZUH_INSTALL_PATH}/etc/sslmanager.key ]
-  then
-    create_wazuh_key_cert
-  fi
-
   # Mount selected files (WAZUH_CONFIG_MOUNT) to container
   mount_files
 
@@ -291,6 +368,12 @@ main() {
 
   # Configure wazuh-manager.conf based on environment variables
   function_configure_wazuh_manager_conf
+
+  # Create the manager server certificates if not present. After mount_files and
+  # the configuration rewrite, so a mounted configuration with custom certificate
+  # paths is honoured and a mounted certificate is detected as already present.
+  create_manager_server_certs
+
   # Delete temporary data folder
   rm -rf ${WAZUH_INSTALL_PATH}/data_tmp
 
diff --git a/build-docker-images/wazuh-manager/config/etc/cont-init.d/1-manager b/build-docker-images/wazuh-manager/config/etc/cont-init.d/1-manager
index 153f2b1c7..23da1bdf4 100644
--- a/build-docker-images/wazuh-manager/config/etc/cont-init.d/1-manager
+++ b/build-docker-images/wazuh-manager/config/etc/cont-init.d/1-manager
@@ -43,11 +43,6 @@ function_wazuh_migration(){
       chown wazuh-manager:wazuh-manager /var/wazuh-manager/etc/client.keys
       chmod 640 /var/wazuh-manager/etc/client.keys
 
-      \cp -f /wazuh-migration/data/etc/sslmanager.cert /var/wazuh-manager/etc/sslmanager.cert
-      \cp -f /wazuh-migration/data/etc/sslmanager.key /var/wazuh-manager/etc/sslmanager.key
-      chown root:root /var/wazuh-manager/etc/sslmanager.cert /var/wazuh-manager/etc/sslmanager.key
-      chmod 640 /var/wazuh-manager/etc/sslmanager.cert /var/wazuh-manager/etc/sslmanager.key
-
       \cp -f /wazuh-migration/data/etc/shared/default/agent.conf /var/wazuh-manager/etc/shared/default/agent.conf
       chown wazuh-manager:wazuh-manager /var/wazuh-manager/etc/shared/default/agent.conf
       chmod 660 /var/wazuh-manager/etc/shared/default/agent.conf
diff --git a/docs/ref/configuration/configuration-files.md b/docs/ref/configuration/configuration-files.md
index e1934003f..64bcab027 100644
--- a/docs/ref/configuration/configuration-files.md
+++ b/docs/ref/configuration/configuration-files.md
@@ -50,6 +50,12 @@ To persist files or directories in your Wazuh deployment, you can mount them as
 
 > **Important**: Ensure that files exist on the host before starting the containers. If the file doesn't exist, Docker will create a directory instead, which may cause startup failures.
 
+### Wazuh manager self-signed certificate
+
+The `docker-compose.yml` files mount a named volume on `/var/wazuh-manager/etc` (`wazuh_etc` in single-node; `master-wazuh-etc` and `worker-wazuh-etc` in multi-node). That volume holds `certs/remoted.pem` and `certs/remoted-key.pem`, the self-signed pair each manager container generates on its first start and reuses on every later start. It is used by the HTTPS agent listener and by agent enrollment (`authd`), and it is unique per deployment and per cluster node.
+
+Removing the volume (for example, with `docker compose down -v`) deletes the pair, and the next start generates a new one. Agents do not validate this certificate by default, so a new pair does not break already enrolled agents. Do not copy the volume between deployments: that reuses the same private key in both. See [Security](../security.md) for rotation and for using your own certificate.
+
 ### Wazuh Dashboard keystore
 
 The `docker-compose.yml` files mount the named volume `wazuh-dashboard-config` on `/usr/share/wazuh-dashboard/config`, which is where `opensearch_dashboards.keystore` is stored. Keeping this volume preserves the `wazuh_ai_assistant.encryptionKey` generated on the first start.
diff --git a/docs/ref/integration_test/docker_integration_tests.md b/docs/ref/integration_test/docker_integration_tests.md
index 6967f5db3..2d7ec42a9 100644
--- a/docs/ref/integration_test/docker_integration_tests.md
+++ b/docs/ref/integration_test/docker_integration_tests.md
@@ -215,7 +215,7 @@ Runs on the **runner** (not the VM):
 
 3. **Copy `wazuh-docker/` to VM** via SCP: `scp -r wazuh-docker {remote}:/tmp/wazuh-docker`
 
-4. **Generate certificates on VM**: runs `tools/utils/deployment/certificates-conf.sh --cert --copy` inside `/tmp/wazuh-docker/{deployment}/`
+4. **Generate certificates on VM**: runs `tools/utils/deployment/certificates-conf.sh --cert --copy --priv` inside `/tmp/wazuh-docker/{deployment}/`
 
 #### Deployment
 
diff --git a/docs/ref/security.md b/docs/ref/security.md
index 7990b8200..95cb4877d 100644
--- a/docs/ref/security.md
+++ b/docs/ref/security.md
@@ -15,6 +15,20 @@ This section summarizes security recommendations for Wazuh Docker deployments (s
 - Regenerate certificates if private keys are leaked or if nodes are re-provisioned.
 - Use certificates and TLS settings appropriate for production (trusted CA, correct DNS names, and key protection).
 
+### Manager self-signed certificate
+
+The Wazuh manager image ships no self-signed certificate. Each manager container generates its own `etc/certs/remoted.pem` and `etc/certs/remoted-key.pem` on its first start, so no two containers share a private key. That pair serves both the HTTPS agent listener and the agent enrollment service (`authd`), and it is stored in the manager `etc` volume (`wazuh_etc` in single-node; `master-wazuh-etc` and `worker-wazuh-etc` in multi-node), which keeps it stable across restarts and container recreation.
+
+- Do not copy or share the manager `etc` volume between deployments, and do not bake the pair into a derived image: either reintroduces a shared private key.
+- To rotate the certificate, remove both files and restart the manager. The next start generates a new pair:
+  ```bash
+  docker compose exec wazuh.manager rm -f /var/wazuh-manager/etc/certs/remoted.pem \
+                                          /var/wazuh-manager/etc/certs/remoted-key.pem
+  docker compose restart wazuh.manager
+  ```
+- To use your own certificate instead, mount the pair at those paths owned by `101:101` (`wazuh-manager:wazuh-manager`) with mode `640`. The container detects it and does not overwrite it. The manager opens these files after dropping privileges, so any other ownership prevents the HTTPS listener from starting.
+- The Wazuh API certificate (`etc/certs/apid.pem` and `apid-key.pem`) is generated by the API on its first start, and is also unique per container.
+
 ## Network exposure
 
 - Restrict access to exposed service ports at the host firewall and security group level.
diff --git a/docs/ref/upgrade.md b/docs/ref/upgrade.md
index effdf23d1..1e3458734 100644
--- a/docs/ref/upgrade.md
+++ b/docs/ref/upgrade.md
@@ -79,3 +79,17 @@ Below is a step-by-step example of how to perform this update:
    ```bash
    docker-compose up -d
    ```
+
+## Manager self-signed certificate on existing deployments
+
+Manager images built before the per-container certificate change shipped `etc/certs/remoted.pem` and `etc/certs/remoted-key.pem` inside the image, so the pair was copied into the manager `etc` volume the first time the deployment started and is the same in every deployment created from that image.
+
+Upgrading the image tag does not replace it: the volume already holds a pair, and the container never overwrites an existing one. To move an existing deployment onto a certificate of its own, remove both files and restart the manager after the upgrade:
+
+```bash
+docker compose exec wazuh.manager rm -f /var/wazuh-manager/etc/certs/remoted.pem \
+                                        /var/wazuh-manager/etc/certs/remoted-key.pem
+docker compose restart wazuh.manager
+```
+
+In multi-node, repeat it for `wazuh.master` and `wazuh.worker`. Agents do not validate this certificate by default, so the rotation does not require any change on the agents.