diff --git a/ee/app/models/remote_development/remote_development_agent_config.rb b/ee/app/models/remote_development/remote_development_agent_config.rb
index 63171b708b74409c16929cf830ec2cc2933d37bb..fc46e59a2b49aba59eb4efdc3fed647b9a3e065b 100644
--- a/ee/app/models/remote_development/remote_development_agent_config.rb
+++ b/ee/app/models/remote_development/remote_development_agent_config.rb
@@ -6,6 +6,8 @@ class RemoteDevelopmentAgentConfig < ApplicationRecord
     #       https://gitlab.com/gitlab-org/gitlab/-/issues/410045#note_1385602915
     include IgnorableColumns
 
+    UNLIMITED_QUOTA = -1
+
     ignore_column :max_workspaces, remove_with: '16.8', remove_after: '2023-12-22'
     ignore_column :max_workspaces_per_user, remove_with: '16.8', remove_after: '2023-12-22'
 
@@ -28,8 +30,9 @@ class RemoteDevelopmentAgentConfig < ApplicationRecord
     validates :max_resources_per_workspace,
       json_schema: { filename: 'remote_development_agent_configs_workspace_container_resources' }
     validates :max_resources_per_workspace, 'remote_development/workspace_container_resources': true
-    validates :workspaces_quota, numericality: { only_integer: true, greater_than_or_equal_to: -1 }
-    validates :workspaces_per_user_quota, numericality: { only_integer: true, greater_than_or_equal_to: -1 }
+    validates :workspaces_quota, numericality: { only_integer: true, greater_than_or_equal_to: UNLIMITED_QUOTA }
+    validates :workspaces_per_user_quota,
+      numericality: { only_integer: true, greater_than_or_equal_to: UNLIMITED_QUOTA }
 
     # noinspection RubyResolve - likely due to https://handbook.gitlab.com/handbook/tools-and-tips/editors-and-ides/jetbrains-ides/tracked-jetbrains-issues/#ruby-25400
     before_validation :prevent_dns_zone_update, if: ->(record) { record.persisted? && record.dns_zone_changed? }
diff --git a/ee/app/models/remote_development/workspace.rb b/ee/app/models/remote_development/workspace.rb
index 49036df610d112d0b31f055a766c2ec706be5515..ce311cba6b51599d6cd609b9ddec80818cd12c96 100644
--- a/ee/app/models/remote_development/workspace.rb
+++ b/ee/app/models/remote_development/workspace.rb
@@ -6,6 +6,7 @@ class Workspace < ApplicationRecord
     include Sortable
     # noinspection RubyResolve - https://handbook.gitlab.com/handbook/tools-and-tips/editors-and-ides/jetbrains-ides/tracked-jetbrains-issues/#ruby-31542
     include RemoteDevelopment::Workspaces::States
+    include ::Gitlab::Utils::StrongMemoize
 
     MAX_HOURS_BEFORE_TERMINATION_LIMIT = 120
 
@@ -39,6 +40,7 @@ class Workspace < ApplicationRecord
     validates :max_hours_before_termination, numericality: { less_than_or_equal_to: MAX_HOURS_BEFORE_TERMINATION_LIMIT }
 
     validate :enforce_permanent_termination
+    validate :enforce_quotas, on: :create
 
     scope :with_desired_state_updated_more_recently_than_last_response_to_agent, -> do
       where('desired_state_updated_at >= responded_to_agent_at').or(where(responded_to_agent_at: nil))
@@ -71,6 +73,43 @@ def desired_state_updated_more_recently_than_last_response_to_agent?
       desired_state_updated_at >= responded_to_agent_at
     end
 
+    def workspaces_count_for_current_user_and_agent
+      Workspace
+        .desired_state_not_terminated
+        .by_user_ids(user_id)
+        .by_agent_ids(cluster_agent_id)
+        .count
+    end
+    strong_memoize_attr :workspaces_count_for_current_user_and_agent
+
+    def workspaces_count_for_current_agent
+      Workspace
+        .desired_state_not_terminated
+        .by_agent_ids(cluster_agent_id)
+        .count
+    end
+    strong_memoize_attr :workspaces_count_for_current_agent
+
+    def exceeds_workspaces_per_user_quota?
+      return unless remote_development_agent_config
+
+      quota = remote_development_agent_config.workspaces_per_user_quota
+      return true if quota == 0
+      return false if quota == -1
+
+      workspaces_count_for_current_user_and_agent >= quota
+    end
+
+    def exceeds_workspaces_quota?
+      return unless remote_development_agent_config
+
+      quota = remote_development_agent_config.workspaces_quota
+      return true if quota == 0
+      return false if quota == -1
+
+      workspaces_count_for_current_agent >= quota
+    end
+
     private
 
     def validate_agent_config_presence
@@ -91,6 +130,23 @@ def enforce_permanent_termination
       errors.add(:desired_state, "is 'Terminated', and cannot be updated. Create a new workspace instead.")
     end
 
+    # rubocop:disable Layout/LineLength  -- Long messages for UI
+    def enforce_quotas
+      agent_config = remote_development_agent_config
+      if exceeds_workspaces_per_user_quota?
+        errors.add :base,
+          format(s_('RemoteDevelopment|You cannot create a workspace because you already have "%{count}" existing workspaces for the given agent with a per user quota of "%{quota}" workspaces'),
+            count: workspaces_count_for_current_user_and_agent,
+            quota: agent_config.workspaces_per_user_quota)
+      elsif exceeds_workspaces_quota?
+        errors.add :base,
+          format(s_('RemoteDevelopment|You cannot create a workspace because there are already "%{count}" existing workspaces for the given agent with a total quota of "%{quota}" workspaces'),
+            count: workspaces_count_for_current_agent,
+            quota: agent_config.workspaces_quota)
+      end
+    end
+    # rubocop:enable Layout/LineLength  -- Long messages for UI
+
     def touch_desired_state_updated_at
       # noinspection RubyResolve - https://handbook.gitlab.com/handbook/tools-and-tips/editors-and-ides/jetbrains-ides/tracked-jetbrains-issues/#ruby-31542
       self.desired_state_updated_at = Time.current.utc
diff --git a/ee/spec/models/remote_development/workspace_spec.rb b/ee/spec/models/remote_development/workspace_spec.rb
index 836fca2809be10364bf3ddd4f1482b5920222a48..cf8453a91e98798d79fa08ac48fb97ef5e78f749 100644
--- a/ee/spec/models/remote_development/workspace_spec.rb
+++ b/ee/spec/models/remote_development/workspace_spec.rb
@@ -156,5 +156,217 @@
           .to include("is 'Terminated', and cannot be updated. Create a new workspace instead.")
       end
     end
+
+    describe "#workspaces_count_for_current_user_and_agent" do
+      let_it_be(:user1) { create(:user) }
+      let_it_be(:user2) { create(:user) }
+      let_it_be(:user3) { create(:user) }
+      let_it_be(:agent1, reload: true) { create(:ee_cluster_agent, :with_remote_development_agent_config) }
+      let_it_be(:agent2, reload: true) { create(:ee_cluster_agent, :with_remote_development_agent_config) }
+      let_it_be(:workspace1) do
+        create(:workspace, user: user1, agent: agent1, desired_state: ::RemoteDevelopment::Workspaces::States::RUNNING)
+      end
+
+      let_it_be(:workspace2) do
+        create(:workspace, user: user2, agent: agent1,
+          desired_state: ::RemoteDevelopment::Workspaces::States::TERMINATED)
+      end
+
+      let_it_be(:workspace3) do
+        create(:workspace, user: user1, agent: agent1, desired_state: ::RemoteDevelopment::Workspaces::States::STOPPED)
+      end
+
+      let_it_be(:workspace4) do
+        create(:workspace, user: user2, agent: agent2,
+          desired_state: ::RemoteDevelopment::Workspaces::States::TERMINATED)
+      end
+
+      let_it_be(:workspace5) do
+        create(:workspace, user: user3, agent: agent2, desired_state: ::RemoteDevelopment::Workspaces::States::RUNNING)
+      end
+
+      it "returns the correct count for the current user and agent" do
+        expect(workspace1.workspaces_count_for_current_user_and_agent).to eq(2)
+        expect(workspace2.workspaces_count_for_current_user_and_agent).to eq(0)
+        expect(workspace4.workspaces_count_for_current_user_and_agent).to eq(0)
+        expect(workspace5.workspaces_count_for_current_user_and_agent).to eq(1)
+      end
+    end
+
+    describe "#workspaces_count_for_current_agent" do
+      let_it_be(:agent1, reload: true) { create(:ee_cluster_agent, :with_remote_development_agent_config) }
+      let_it_be(:agent2, reload: true) { create(:ee_cluster_agent, :with_remote_development_agent_config) }
+      let_it_be(:workspace1) do
+        create(:workspace, agent: agent1,  desired_state: ::RemoteDevelopment::Workspaces::States::RUNNING)
+      end
+
+      let_it_be(:workspace2) do
+        create(:workspace, agent: agent1,  desired_state: ::RemoteDevelopment::Workspaces::States::TERMINATED)
+      end
+
+      let_it_be(:workspace3) do
+        create(:workspace, agent: agent1,  desired_state: ::RemoteDevelopment::Workspaces::States::STOPPED)
+      end
+
+      let_it_be(:workspace4) do
+        create(:workspace, agent: agent2,  desired_state: ::RemoteDevelopment::Workspaces::States::TERMINATED)
+      end
+
+      let_it_be(:workspace5) do
+        create(:workspace, agent: agent2,  desired_state: ::RemoteDevelopment::Workspaces::States::RUNNING)
+      end
+
+      it "returns the correct count for the current agent" do
+        expect(workspace1.workspaces_count_for_current_agent).to eq(2)
+        expect(workspace4.workspaces_count_for_current_agent).to eq(1)
+        expect(workspace5.workspaces_count_for_current_agent).to eq(1)
+      end
+    end
+
+    describe "#exceeds_workspaces_per_user_quota?" do
+      let(:workspace) { create(:workspace) }
+
+      context "when remote_development_agent_config is nil" do
+        it "returns false" do
+          workspace.remote_development_agent_config = nil
+          expect(workspace.exceeds_workspaces_per_user_quota?).to be nil
+        end
+      end
+
+      context "when remote_development_agent_config is present" do
+        context "when workspaces_per_user_quota is 0" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_per_user_quota: 0))
+          end
+
+          it "returns true" do
+            expect(workspace.exceeds_workspaces_per_user_quota?).to be true
+          end
+        end
+
+        context "when workspaces_per_user_quota is -1" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_per_user_quota: -1))
+          end
+
+          it "returns false" do
+            expect(workspace.exceeds_workspaces_per_user_quota?).to be false
+          end
+        end
+
+        context "when workspaces_per_user_quota is greater than 0" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_per_user_quota: 2))
+          end
+
+          it "returns true if the workspaces count for current user and agent is greater than or equal to the quota" do
+            allow(workspace).to receive(:workspaces_count_for_current_user_and_agent).and_return(3)
+            expect(workspace.exceeds_workspaces_per_user_quota?).to be true
+          end
+
+          it "returns false if the workspaces count for current user and agent is less than the quota" do
+            allow(workspace).to receive(:workspaces_count_for_current_user_and_agent).and_return(1)
+            expect(workspace.exceeds_workspaces_per_user_quota?).to be false
+          end
+        end
+      end
+    end
+
+    describe "#exceeds_workspaces_quota?" do
+      let(:workspace) { create(:workspace) }
+
+      context "when remote_development_agent_config is nil" do
+        it "returns false" do
+          workspace.remote_development_agent_config = nil
+          expect(workspace.exceeds_workspaces_quota?).to be nil
+        end
+      end
+
+      context "when remote_development_agent_config is present" do
+        context "when workspaces_quota is 0" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_quota: 0))
+          end
+
+          it "returns true" do
+            expect(workspace.exceeds_workspaces_quota?).to be true
+          end
+        end
+
+        context "when workspaces_quota is -1" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_quota: -1))
+          end
+
+          it "returns false" do
+            expect(workspace.exceeds_workspaces_quota?).to be false
+          end
+        end
+
+        context "when workspaces_quota is greater than 0" do
+          before do
+            allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+              RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_quota: 2))
+          end
+
+          it "returns true if the workspaces count for the current agent is greater than or equal to the quota" do
+            allow(workspace).to receive(:workspaces_count_for_current_agent).and_return(3)
+            expect(workspace.exceeds_workspaces_quota?).to be true
+          end
+
+          it "returns false if the workspaces count for the current agent is less than the quota" do
+            allow(workspace).to receive(:workspaces_count_for_current_agent).and_return(1)
+            expect(workspace.exceeds_workspaces_quota?).to be false
+          end
+        end
+      end
+    end
+
+    describe '#enforce_quotas' do
+      subject(:workspace) do
+        build(:workspace,
+          user: user,
+          agent: agent,
+          project: project,
+          personal_access_token: personal_access_token, desired_state: desired_state)
+      end
+
+      before do
+        allow(workspace).to receive(:exceeds_workspaces_per_user_quota?).and_return(false)
+        allow(workspace).to receive(:exceeds_workspaces_quota?).and_return(false)
+      end
+
+      it 'does not add base errors when quotas are not exceeded' do
+        workspace.validate
+        expect(workspace.errors[:base]).to be_empty
+      end
+
+      it 'adds base error when per user quota exceeded' do
+        allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+          ::RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_per_user_quota: 5))
+        allow(workspace).to receive(:workspaces_count_for_current_user_and_agent).and_return(6)
+        allow(workspace).to receive(:exceeds_workspaces_per_user_quota?).and_return(true)
+        workspace.validate
+        message = "You cannot create a workspace because you already have \"6\" \
+existing workspaces for the given agent with a per user quota of \"5\" workspaces"
+        expect(workspace.errors[:base]).to include(message)
+      end
+
+      it 'adds base error when total quota exceeded' do
+        allow(workspace).to receive(:remote_development_agent_config).and_return(instance_double(
+          ::RemoteDevelopment::RemoteDevelopmentAgentConfig, workspaces_quota: 3))
+        allow(workspace).to receive(:workspaces_count_for_current_agent).and_return(3)
+        allow(workspace).to receive(:exceeds_workspaces_quota?).and_return(true)
+        workspace.validate
+        message = "You cannot create a workspace because there are already \"3\" \
+existing workspaces for the given agent with a total quota of \"3\" workspaces"
+        expect(workspace.errors[:base]).to include(message)
+      end
+    end
   end
 end
diff --git a/locale/gitlab.pot b/locale/gitlab.pot
index b41845620a11932f1431037c4d00a5e1993d7915..27092459c2a7e84df187e42d56c548b2454069bf 100644
--- a/locale/gitlab.pot
+++ b/locale/gitlab.pot
@@ -40542,6 +40542,12 @@ msgstr ""
 msgid "RemoteDevelopment|Workspaces"
 msgstr ""
 
+msgid "RemoteDevelopment|You cannot create a workspace because there are already \"%{count}\" existing workspaces for the given agent with a total quota of \"%{quota}\" workspaces"
+msgstr ""
+
+msgid "RemoteDevelopment|You cannot create a workspace because you already have \"%{count}\" existing workspaces for the given agent with a per user quota of \"%{quota}\" workspaces"
+msgstr ""
+
 msgid "Remove"
 msgstr ""