diff --git a/app/lib/proxy_api/remote_execution_ssh.rb b/app/lib/proxy_api/remote_execution_ssh.rb
index 8b755d27b..a68330af3 100644
--- a/app/lib/proxy_api/remote_execution_ssh.rb
+++ b/app/lib/proxy_api/remote_execution_ssh.rb
@@ -11,6 +11,12 @@ def pubkey
       raise ProxyException.new(url, e, N_('Unable to fetch public key'))
     end
 
+    def ca_pubkey
+      get('ca_pubkey')&.strip
+    rescue => e
+      raise ProxyException.new(url, e, N_('Unable to fetch CA public key'))
+    end
+
     def drop_from_known_hosts(hostname)
       delete('known_hosts/' + hostname)
     rescue => e
diff --git a/app/models/concerns/foreman_remote_execution/host_extensions.rb b/app/models/concerns/foreman_remote_execution/host_extensions.rb
index 35fb32e28..ebbd7fa27 100644
--- a/app/models/concerns/foreman_remote_execution/host_extensions.rb
+++ b/app/models/concerns/foreman_remote_execution/host_extensions.rb
@@ -108,7 +108,12 @@ def remote_execution_proxies(provider, authorized = true)
     end
 
     def remote_execution_ssh_keys
-      remote_execution_proxies(%w(SSH Script), false).values.flatten.uniq.map { |proxy| proxy.pubkey }.compact.uniq
+      # only include public keys from SSH proxies that don't have SSH cert verification configured
+      remote_execution_proxies(%w(SSH Script), false).values.flatten.uniq.map { |proxy| proxy.pubkey if proxy.ca_pubkey.blank? }.compact.uniq
+    end
+
+    def remote_execution_ssh_ca_keys
+      remote_execution_proxies(%w(SSH Script), false).values.flatten.uniq.map { |proxy| proxy.ca_pubkey }.compact.uniq
     end
 
     def drop_execution_interface_cache
@@ -139,10 +144,13 @@ def infrastructure_host?
 
     def extend_host_params_hash(params)
       keys = remote_execution_ssh_keys
+      ca_keys = remote_execution_ssh_ca_keys
       source = 'global'
-      if keys.present?
-        value, safe_value = params.fetch('remote_execution_ssh_keys', {}).values_at(:value, :safe_value).map { |v| [v].flatten.compact }
-        params['remote_execution_ssh_keys'] = {:value => value + keys, :safe_value => safe_value + keys, :source => source}
+      {keys: keys, ca_keys: ca_keys}.each do |key_set_name, key_set|
+        if key_set.present?
+          value, safe_value = params.fetch("remote_execution_ssh_#{key_set_name}", {}).values_at(:value, :safe_value).map { |v| [v].flatten.compact }
+          params["remote_execution_ssh_#{key_set_name}"] = {:value => value + key_set, :safe_value => safe_value + key_set, :source => source}
+        end
       end
       [:remote_execution_ssh_user, :remote_execution_effective_user_method,
        :remote_execution_connect_by_ip].each do |key|
diff --git a/app/models/concerns/foreman_remote_execution/smart_proxy_extensions.rb b/app/models/concerns/foreman_remote_execution/smart_proxy_extensions.rb
index 163b21b36..9d2ac8091 100644
--- a/app/models/concerns/foreman_remote_execution/smart_proxy_extensions.rb
+++ b/app/models/concerns/foreman_remote_execution/smart_proxy_extensions.rb
@@ -11,6 +11,10 @@ def pubkey
       self[:pubkey] || update_pubkey
     end
 
+    def ca_pubkey
+      self[:ca_pubkey] || update_ca_pubkey
+    end
+
     def update_pubkey
       return unless has_feature?(%w(SSH Script))
 
@@ -19,6 +23,15 @@ def update_pubkey
       key
     end
 
+    def update_ca_pubkey
+      return unless has_feature?(%w(SSH Script))
+
+      # smart proxy is not required to have a CA pubkey, in which case an empty string is returned
+      key = ::ProxyAPI::RemoteExecutionSSH.new(:url => url).ca_pubkey&.presence
+      self.update_attribute(:ca_pubkey, key)
+      key
+    end
+
     def drop_host_from_known_hosts(host)
       ::ProxyAPI::RemoteExecutionSSH.new(:url => url).drop_from_known_hosts(host)
     end
@@ -26,6 +39,7 @@ def drop_host_from_known_hosts(host)
     def refresh
       errors = super
       update_pubkey
+      update_ca_pubkey
       errors
     end
   end
diff --git a/app/views/api/v2/smart_proxies/ca_pubkey.json.rabl b/app/views/api/v2/smart_proxies/ca_pubkey.json.rabl
new file mode 100644
index 000000000..fd13aae3a
--- /dev/null
+++ b/app/views/api/v2/smart_proxies/ca_pubkey.json.rabl
@@ -0,0 +1 @@
+attribute :ca_pubkey => :remote_execution_ca_pubkey
diff --git a/db/migrate/20250606125543_add_ca_pub_key_to_smart_proxy.rb b/db/migrate/20250606125543_add_ca_pub_key_to_smart_proxy.rb
new file mode 100644
index 000000000..f5a189770
--- /dev/null
+++ b/db/migrate/20250606125543_add_ca_pub_key_to_smart_proxy.rb
@@ -0,0 +1,5 @@
+class AddCAPubKeyToSmartProxy < ActiveRecord::Migration[7.0]
+  def change
+    add_column :smart_proxies, :ca_pubkey, :text
+  end
+end
diff --git a/lib/foreman_remote_execution/plugin.rb b/lib/foreman_remote_execution/plugin.rb
index 69a5241a4..3dace7a7f 100644
--- a/lib/foreman_remote_execution/plugin.rb
+++ b/lib/foreman_remote_execution/plugin.rb
@@ -213,6 +213,7 @@
   extend_template_helpers ForemanRemoteExecution::RendererMethods
 
   extend_rabl_template 'api/v2/smart_proxies/main', 'api/v2/smart_proxies/pubkey'
+  extend_rabl_template 'api/v2/smart_proxies/main', 'api/v2/smart_proxies/ca_pubkey'
   extend_rabl_template 'api/v2/interfaces/main', 'api/v2/interfaces/execution_flag'
   extend_rabl_template 'api/v2/subnets/show', 'api/v2/subnets/remote_execution_proxies'
   extend_rabl_template 'api/v2/hosts/main', 'api/v2/host/main'
diff --git a/test/unit/concerns/host_extensions_test.rb b/test/unit/concerns/host_extensions_test.rb
index ae4bfe950..c493d0604 100644
--- a/test/unit/concerns/host_extensions_test.rb
+++ b/test/unit/concerns/host_extensions_test.rb
@@ -12,6 +12,7 @@ class ForemanRemoteExecutionHostExtensionsTest < ActiveSupport::TestCase
 
     before do
       SmartProxy.any_instance.stubs(:pubkey).returns(sshkey)
+      SmartProxy.any_instance.stubs(:ca_pubkey).returns(nil)
       Setting[:remote_execution_ssh_user] = 'root'
       Setting[:remote_execution_effective_user_method] = 'sudo'
     end
@@ -61,6 +62,48 @@ class ForemanRemoteExecutionHostExtensionsTest < ActiveSupport::TestCase
     end
   end
 
+  describe 'has ssh CA key configured' do
+    let(:host) { FactoryBot.create(:host, :with_execution) }
+    let(:sshkey) { 'ssh-rsa AAAAB3NzaC1yc2EAAAABJQ foo@example.com' }
+    let(:ca_sshkey) { 'ssh-rsa AAAAB3NzaC1yc2EAAAABJE bar@example.com' }
+
+    before do
+      SmartProxy.any_instance.stubs(:pubkey).returns(sshkey)
+      SmartProxy.any_instance.stubs(:ca_pubkey).returns(ca_sshkey)
+      Setting[:remote_execution_ssh_user] = 'root'
+      Setting[:remote_execution_effective_user_method] = 'sudo'
+    end
+
+    it 'has CA ssh keys in the parameters' do
+      assert_includes host.remote_execution_ssh_ca_keys, ca_sshkey
+    end
+
+    it 'excludes ssh keys from proxies that have SSH CA key configured' do
+      assert_empty host.remote_execution_ssh_keys
+    end
+
+    it 'merges ssh CA keys from host parameters and proxies' do
+      key = 'ssh-rsa not-even-a-key something@somewhere.com'
+      host.host_parameters << FactoryBot.create(:host_parameter, :host => host, :name => 'remote_execution_ssh_ca_keys', :value => [key])
+      assert_includes host.host_param('remote_execution_ssh_ca_keys'), key
+      assert_includes host.host_param('remote_execution_ssh_ca_keys'), ca_sshkey
+    end
+
+    it 'has ssh CA keys in the parameters even when no user specified' do
+      FactoryBot.create(:smart_proxy, :ssh)
+      host.interfaces.first.subnet.remote_execution_proxies.clear
+      User.current = nil
+      assert_includes host.remote_execution_ssh_ca_keys, ca_sshkey
+    end
+
+    it 'merges ssh CA key as a string from host parameters and proxies' do
+      key = 'ssh-rsa not-even-a-key something@somewhere.com'
+      host.host_parameters << FactoryBot.create(:host_parameter, :host => host, :name => 'remote_execution_ssh_ca_keys', :value => key)
+      assert_includes host.host_param('remote_execution_ssh_ca_keys'), key
+      assert_includes host.host_param('remote_execution_ssh_ca_keys'), ca_sshkey
+    end
+  end
+
   context 'host has multiple nics' do
     let(:host) { FactoryBot.build(:host, :with_execution) }