diff --git a/changes/19464-private-key-errors b/changes/19464-private-key-errors
new file mode 100644
index 0000000000..ddd0fd2f65
--- /dev/null
+++ b/changes/19464-private-key-errors
@@ -0,0 +1 @@
+- Adds clearer error messages when attempting to set up Apple MDM without a server private key configured.
\ No newline at end of file
diff --git a/frontend/pages/admin/IntegrationsPage/cards/MdmSettings/MacOSMdmPage/components/content/ApplePushCertSetup.tsx b/frontend/pages/admin/IntegrationsPage/cards/MdmSettings/MacOSMdmPage/components/content/ApplePushCertSetup.tsx
index 8eb0ea88d5..272c74f75c 100644
--- a/frontend/pages/admin/IntegrationsPage/cards/MdmSettings/MacOSMdmPage/components/content/ApplePushCertSetup.tsx
+++ b/frontend/pages/admin/IntegrationsPage/cards/MdmSettings/MacOSMdmPage/components/content/ApplePushCertSetup.tsx
@@ -32,7 +32,10 @@ const ApplePushCertSetup = ({
         onSetupSuccess();
       } catch (e) {
         const msg = getErrorReason(e);
-        if (msg.toLowerCase().includes("invalid certificate")) {
+        if (
+          msg.toLowerCase().includes("invalid certificate") ||
+          msg.toLowerCase().includes("required private key")
+        ) {
           renderFlash("error", msg);
         } else {
           renderFlash("error", "Couldn’t connect. Please try again.");
@@ -46,7 +49,10 @@ const ApplePushCertSetup = ({
   const onDownloadError = useCallback(
     (e: unknown) => {
       const msg = getErrorReason(e);
-      if (msg.toLowerCase().includes("email address")) {
+      if (
+        msg.toLowerCase().includes("email address") ||
+        msg.toLowerCase().includes("required private key")
+      ) {
         renderFlash("error", msg);
       } else {
         renderFlash("error", "Something’s gone wrong. Please try again.");
diff --git a/frontend/pages/admin/components/DownloadFileButtons/DownloadABMKey.tsx b/frontend/pages/admin/components/DownloadFileButtons/DownloadABMKey.tsx
index 70df97ea3e..891ea45a58 100644
--- a/frontend/pages/admin/components/DownloadFileButtons/DownloadABMKey.tsx
+++ b/frontend/pages/admin/components/DownloadFileButtons/DownloadABMKey.tsx
@@ -1,6 +1,14 @@
-import React, { FormEvent, useCallback, useMemo, useState } from "react";
+import React, {
+  FormEvent,
+  useCallback,
+  useMemo,
+  useState,
+  useContext,
+} from "react";
 
 import mdmAppleBusinessManagerApi from "services/entities/mdm_apple_bm";
+import { NotificationContext } from "context/notification";
+import { getErrorReason } from "interfaces/errors";
 
 import Icon from "components/Icon";
 import Button from "components/buttons/Button";
@@ -23,6 +31,7 @@ const useDownloadABMKey = ({
   onError,
 }: Omit<IDownloadABMKeyProps, "baseClass">) => {
   const [downloadState, setDownloadState] = useState<RequestState>(undefined);
+  const { renderFlash } = useContext(NotificationContext);
 
   const handleDownload = useCallback(
     async (evt: FormEvent) => {
@@ -34,6 +43,8 @@ const useDownloadABMKey = ({
         setDownloadState("success");
         onSuccess && onSuccess();
       } catch (e) {
+        const msg = getErrorReason(e);
+        renderFlash("error", msg);
         setDownloadState("error");
         onError && onError(e);
       }
diff --git a/server/service/apple_mdm.go b/server/service/apple_mdm.go
index aaf2a4a505..9799f6e7e0 100644
--- a/server/service/apple_mdm.go
+++ b/server/service/apple_mdm.go
@@ -3592,6 +3592,16 @@ func (svc *Service) GenerateABMKeyPair(ctx context.Context) (*fleet.MDMAppleDEPK
 	if err := svc.authz.Authorize(ctx, &fleet.AppleBM{}, fleet.ActionWrite); err != nil {
 		return nil, err
 	}
+
+	privateKey := svc.config.Server.PrivateKey
+	if testSetEmptyPrivateKey {
+		privateKey = ""
+	}
+
+	if len(privateKey) == 0 {
+		return nil, ctxerr.New(ctx, "Couldn't download public key. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
+	}
+
 	var publicKeyPEM, privateKeyPEM []byte
 	assets, err := svc.ds.GetAllMDMConfigAssetsByName(ctx, []fleet.MDMAssetName{
 		fleet.MDMAssetABMCert,
diff --git a/server/service/integration_mdm_test.go b/server/service/integration_mdm_test.go
index 512bef6e76..4463ab2cda 100644
--- a/server/service/integration_mdm_test.go
+++ b/server/service/integration_mdm_test.go
@@ -936,6 +936,15 @@ func (s *integrationMDMTestSuite) TestGetMDMCSR() {
 	t := s.T()
 	ctx := context.Background()
 
+	// Validate errors if no private key is set
+	testSetEmptyPrivateKey = true
+	t.Cleanup(func() { testSetEmptyPrivateKey = false })
+	s.uploadAPNSCert([]byte("-----BEGIN CERTIFICATE-----\nZm9vCg==\n-----END CERTIFICATE-----"), http.StatusInternalServerError, "Couldn't upload APNs certificate. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
+
+	r := s.Do("GET", "/api/latest/fleet/mdm/apple/request_csr", getMDMAppleCSRRequest{}, http.StatusInternalServerError)
+	require.Contains(t, extractServerErrorText(r.Body), "Couldn't download signed CSR. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
+	testSetEmptyPrivateKey = false
+
 	// ensure we leave everything in a clean state for other tests
 	t.Cleanup(s.appleCoreCertsSetup)
 
@@ -8674,6 +8683,14 @@ func (s *integrationMDMTestSuite) TestABMAssetManagement() {
 	// ensure enable ABM again for other tests
 	t.Cleanup(s.enableABM)
 
+	// Validate error when server private key not set
+	testSetEmptyPrivateKey = true
+	t.Cleanup(func() { testSetEmptyPrivateKey = false })
+
+	r := s.Do("GET", "/api/latest/fleet/mdm/apple/abm_public_key", generateABMKeyPairResponse{}, http.StatusInternalServerError)
+	require.Contains(t, extractServerErrorText(r.Body), "Couldn't download public key. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
+	testSetEmptyPrivateKey = false
+
 	// grab the current public key
 	var abmResp generateABMKeyPairResponse
 	s.DoJSON("GET", "/api/latest/fleet/mdm/apple/abm_public_key", nil, http.StatusOK, &abmResp)
diff --git a/server/service/mdm.go b/server/service/mdm.go
index b631f6818d..069a5ecf1d 100644
--- a/server/service/mdm.go
+++ b/server/service/mdm.go
@@ -2120,6 +2120,9 @@ func (svc *Service) ResendHostMDMProfile(ctx context.Context, hostID uint, profi
 // GET /mdm/apple/request_csr
 ////////////////////////////////////////////////////////////////////////////////
 
+// Used for overriding the env var value in testing
+var testSetEmptyPrivateKey bool
+
 type getMDMAppleCSRRequest struct{}
 
 type getMDMAppleCSRResponse struct {
@@ -2143,8 +2146,13 @@ func (svc *Service) GetMDMAppleCSR(ctx context.Context) ([]byte, error) {
 		return nil, err
 	}
 
-	if len(svc.config.Server.PrivateKey) == 0 {
-		return nil, ctxerr.New(ctx, "no private key configured")
+	privateKey := svc.config.Server.PrivateKey
+	if testSetEmptyPrivateKey {
+		privateKey = ""
+	}
+
+	if len(privateKey) == 0 {
+		return nil, ctxerr.New(ctx, "Couldn't download signed CSR. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
 	}
 
 	vc, ok := viewer.FromContext(ctx)
@@ -2298,6 +2306,15 @@ func (svc *Service) UploadMDMAppleAPNSCert(ctx context.Context, cert io.ReadSeek
 		return err
 	}
 
+	privateKey := svc.config.Server.PrivateKey
+	if testSetEmptyPrivateKey {
+		privateKey = ""
+	}
+
+	if len(privateKey) == 0 {
+		return ctxerr.New(ctx, "Couldn't upload APNs certificate. Missing required private key. Learn how to configure the private key here: https://fleetdm.com/learn-more-about/fleet-server-private-key")
+	}
+
 	if cert == nil {
 		return ctxerr.Wrap(ctx, fleet.NewInvalidArgumentError("certificate", "Invalid certificate. Please provide a valid certificate from Apple Push Certificate Portal."))
 	}