diff --git a/server/datastore/mysql/microsoft_mdm.go b/server/datastore/mysql/microsoft_mdm.go
index fb128f612c..8174b0aae9 100644
--- a/server/datastore/mysql/microsoft_mdm.go
+++ b/server/datastore/mysql/microsoft_mdm.go
@@ -1,6 +1,7 @@
 package mysql
 
 import (
+	"bytes"
 	"context"
 	"database/sql"
 	"encoding/xml"
@@ -18,6 +19,11 @@ import (
 	"github.com/jmoiron/sqlx"
 )
 
+// windowsMDMProfileDeleteBatchSize is the number of hosts to process per
+// batch when enqueuing <Delete> commands and updating host profile rows
+// during profile deletion.
+const windowsMDMProfileDeleteBatchSize = 5000
+
 func isWindowsHostConnectedToFleetMDM(ctx context.Context, q sqlx.QueryerContext, h *fleet.Host) (bool, error) {
 	var unused string
 
@@ -378,12 +384,32 @@ func (ds *Datastore) MDMWindowsInsertCommandForHosts(ctx context.Context, hostUU
 	})
 }
 
-func (ds *Datastore) mdmWindowsInsertCommandForHostsDB(ctx context.Context, tx sqlx.ExecerContext, hostUUIDsOrDeviceIDs []string, cmd *fleet.MDMWindowsCommand) error {
-	// first, create the command entry
-	stmt := `
-		INSERT INTO windows_mdm_commands (command_uuid, raw_command, target_loc_uri)
-		VALUES (?, ?, ?)
-  `
+func (ds *Datastore) mdmWindowsInsertCommandForHostsDB(ctx context.Context, tx sqlx.ExtContext, hostUUIDsOrDeviceIDs []string, cmd *fleet.MDMWindowsCommand) error {
+	// Resolve host UUIDs / device IDs to enrollment IDs using the general-purpose
+	// lookup (supports both host_uuid and mdm_device_id via subquery).
+	enrollmentIDs, err := ds.getEnrollmentIDsByHostUUIDOrDeviceIDDB(ctx, tx, hostUUIDsOrDeviceIDs)
+	if err != nil {
+		return ctxerr.Wrap(ctx, err, "fetching enrollment IDs for command queue")
+	}
+	return ds.mdmWindowsInsertCommandForEnrollmentIDsDB(ctx, tx, enrollmentIDs, cmd)
+}
+
+// mdmWindowsInsertCommandForHostUUIDsDB is the fast path for bulk operations
+// that always have host UUIDs (not device IDs). Uses an indexed batch SELECT
+// instead of per-row subqueries.
+func (ds *Datastore) mdmWindowsInsertCommandForHostUUIDsDB(ctx context.Context, tx sqlx.ExtContext, hostUUIDs []string, cmd *fleet.MDMWindowsCommand) error {
+	enrollmentIDs, err := ds.getEnrollmentIDsByHostUUIDDB(ctx, tx, hostUUIDs)
+	if err != nil {
+		return ctxerr.Wrap(ctx, err, "fetching enrollment IDs by host UUID")
+	}
+	return ds.mdmWindowsInsertCommandForEnrollmentIDsDB(ctx, tx, enrollmentIDs, cmd)
+}
+
+// mdmWindowsInsertCommandForEnrollmentIDsDB inserts the command and queues it
+// for the given enrollment IDs.
+func (ds *Datastore) mdmWindowsInsertCommandForEnrollmentIDsDB(ctx context.Context, tx sqlx.ExtContext, enrollmentIDs []uint, cmd *fleet.MDMWindowsCommand) error {
+	// Create the command entry.
+	stmt := `INSERT INTO windows_mdm_commands (command_uuid, raw_command, target_loc_uri) VALUES (?, ?, ?)`
 	if _, err := tx.ExecContext(ctx, stmt, cmd.CommandUUID, cmd.RawCommand, cmd.TargetLocURI); err != nil {
 		if IsDuplicate(err) {
 			return ctxerr.Wrap(ctx, alreadyExists("MDMWindowsCommand", cmd.CommandUUID))
@@ -391,29 +417,68 @@ func (ds *Datastore) mdmWindowsInsertCommandForHostsDB(ctx context.Context, tx s
 		return ctxerr.Wrap(ctx, err, "inserting MDMWindowsCommand")
 	}
 
-	// create the command execution queue entries, one per host
-	for _, hostUUIDOrDeviceID := range hostUUIDsOrDeviceIDs {
-		if err := ds.mdmWindowsInsertHostCommandDB(ctx, tx, hostUUIDOrDeviceID, cmd.CommandUUID); err != nil {
-			return err
-		}
+	if len(enrollmentIDs) == 0 {
+		return nil
 	}
-	return nil
+
+	// Batch insert into command queue.
+	return common_mysql.BatchProcessSimple(enrollmentIDs, windowsMDMProfileDeleteBatchSize, func(batch []uint) error {
+		valuesPart := strings.Repeat("(?, ?),", len(batch))
+		valuesPart = strings.TrimSuffix(valuesPart, ",")
+
+		args := make([]any, 0, len(batch)*2)
+		for _, eid := range batch {
+			args = append(args, eid, cmd.CommandUUID)
+		}
+
+		batchStmt := `INSERT INTO windows_mdm_command_queue (enrollment_id, command_uuid) VALUES ` + valuesPart
+		if _, err := tx.ExecContext(ctx, batchStmt, args...); err != nil {
+			return ctxerr.Wrap(ctx, err, "batch inserting MDMWindowsCommandQueue")
+		}
+		return nil
+	})
 }
 
-func (ds *Datastore) mdmWindowsInsertHostCommandDB(ctx context.Context, tx sqlx.ExecerContext, hostUUIDOrDeviceID, commandUUID string) error {
-	stmt := `
-INSERT INTO windows_mdm_command_queue (enrollment_id, command_uuid)
-VALUES ((SELECT id FROM mdm_windows_enrollments WHERE host_uuid = ? OR mdm_device_id = ? ORDER BY created_at DESC LIMIT 1), ?)
-`
-
-	if _, err := tx.ExecContext(ctx, stmt, hostUUIDOrDeviceID, hostUUIDOrDeviceID, commandUUID); err != nil {
-		if IsDuplicate(err) {
-			return ctxerr.Wrap(ctx, alreadyExists("MDMWindowsCommandQueue", commandUUID))
+// getEnrollmentIDsByHostUUIDDB fetches enrollment IDs for a list of host UUIDs
+// using an indexed batch query. Returns the most recent enrollment per host.
+func (ds *Datastore) getEnrollmentIDsByHostUUIDDB(ctx context.Context, tx sqlx.ExtContext, hostUUIDs []string) ([]uint, error) {
+	var allIDs []uint
+	err := common_mysql.BatchProcessSimple(hostUUIDs, windowsMDMProfileDeleteBatchSize, func(batch []string) error {
+		stmt, args, err := sqlx.In(
+			`SELECT MAX(id) FROM mdm_windows_enrollments WHERE host_uuid IN (?) GROUP BY host_uuid`,
+			batch)
+		if err != nil {
+			return err
 		}
-		return ctxerr.Wrap(ctx, err, "inserting MDMWindowsCommandQueue", "host_uuid_or_device_id", hostUUIDOrDeviceID, "command_uuid", commandUUID)
-	}
+		var ids []uint
+		if err := sqlx.SelectContext(ctx, tx, &ids, stmt, args...); err != nil {
+			return err
+		}
+		allIDs = append(allIDs, ids...)
+		return nil
+	})
+	return allIDs, err
+}
 
-	return nil
+// getEnrollmentIDsByHostUUIDOrDeviceIDDB fetches enrollment IDs using a
+// per-row SELECT that supports both host_uuid and mdm_device_id lookups.
+// Used by the general-purpose command insertion path (typically 1-2 IDs).
+func (ds *Datastore) getEnrollmentIDsByHostUUIDOrDeviceIDDB(ctx context.Context, tx sqlx.ExtContext, hostUUIDsOrDeviceIDs []string) ([]uint, error) {
+	var allIDs []uint
+	for _, id := range hostUUIDsOrDeviceIDs {
+		var eid uint
+		err := sqlx.GetContext(ctx, tx, &eid,
+			`SELECT id FROM mdm_windows_enrollments WHERE host_uuid = ? OR mdm_device_id = ? ORDER BY created_at DESC LIMIT 1`,
+			id, id)
+		if err != nil {
+			if errors.Is(err, sql.ErrNoRows) {
+				continue // host not enrolled, skip
+			}
+			return nil, ctxerr.Wrap(ctx, err, "looking up enrollment ID")
+		}
+		allIDs = append(allIDs, eid)
+	}
+	return allIDs, nil
 }
 
 // MDMWindowsGetPendingCommands retrieves all commands awaiting execution for a
@@ -448,6 +513,8 @@ WHERE
 			wmcr.enrollment_id = wmcq.enrollment_id AND
 			wmcr.command_uuid = wmcq.command_uuid
 	)
+ORDER BY
+	wmc.created_at ASC
 `
 
 	if err := sqlx.SelectContext(ctx, ds.reader(ctx), &commands, query, deviceID); err != nil {
@@ -559,7 +626,7 @@ func (ds *Datastore) MDMWindowsSaveResponse(ctx context.Context, deviceID string
 					pp, err := fleet.BuildMDMWindowsProfilePayloadFromMDMResponse(cmdWithSecret, enrichedSyncML.CmdRefUUIDToStatus,
 						enrolledDevice.HostUUID, cmdOperationTypes[cmd.CommandUUID] == fleet.MDMOperationTypeRemove)
 					if err != nil {
-						return err
+						return ctxerr.Wrap(ctx, err, "building profile payload from MDM response")
 					}
 					potentialProfilePayloads = append(potentialProfilePayloads, pp)
 				}
@@ -1201,15 +1268,18 @@ func (ds *Datastore) cancelWindowsHostInstallsForDeletedMDMProfiles(
 	// This prevents deleting one profile from undoing settings in another.
 	activeLocURIs := make(map[string]bool)
 	if len(profileUUIDs) > 0 {
-		// Get team IDs for the profiles being deleted (from host assignments).
+		// Get team IDs for the profiles being deleted. Use the hosts table
+		// with a single query instead of one per host.
+		teamIDStmt, teamIDArgs, err := sqlx.In(
+			`SELECT DISTINCT COALESCE(h.team_id, 0) FROM hosts h
+			JOIN host_mdm_windows_profiles hwp ON hwp.host_uuid = h.uuid
+			WHERE hwp.profile_uuid IN (?)`, profileUUIDs)
+		if err != nil {
+			return ctxerr.Wrap(ctx, err, "building IN for team ID lookup")
+		}
 		var teamIDs []uint
-		for _, row := range rowsToRemove {
-			// Look up team from the host.
-			var teamID uint
-			if err := sqlx.GetContext(ctx, tx, &teamID,
-				`SELECT COALESCE(team_id, 0) FROM hosts WHERE uuid = ?`, row.HostUUID); err == nil {
-				teamIDs = append(teamIDs, teamID)
-			}
+		if err := sqlx.SelectContext(ctx, tx, &teamIDs, teamIDStmt, teamIDArgs...); err != nil {
+			return ctxerr.Wrap(ctx, err, "selecting team IDs for LocURI protection")
 		}
 		if len(teamIDs) > 0 {
 			// Query all SyncML from profiles NOT being deleted in the same team(s).
@@ -1221,14 +1291,8 @@ func (ds *Datastore) cancelWindowsHostInstallsForDeletedMDMProfiles(
 				var activeProfiles [][]byte
 				if err := sqlx.SelectContext(ctx, tx, &activeProfiles, apStmt, apArgs...); err == nil {
 					for _, syncML := range activeProfiles {
-						cmds, err := fleet.UnmarshallMultiTopLevelXMLProfile(syncML)
-						if err != nil {
-							continue
-						}
-						for _, cmd := range cmds {
-							if uri := cmd.GetTargetURI(); uri != "" {
-								activeLocURIs[uri] = true
-							}
+						for _, uri := range fleet.ExtractLocURIsFromProfileBytes(syncML) {
+							activeLocURIs[uri] = true
 						}
 					}
 				}
@@ -1268,7 +1332,7 @@ func (ds *Datastore) cancelWindowsHostInstallsForDeletedMDMProfiles(
 			continue
 		}
 
-		if err := ds.mdmWindowsInsertCommandForHostsDB(ctx, tx, target.hostUUIDs, deleteCmd); err != nil {
+		if err := ds.mdmWindowsInsertCommandForHostUUIDsDB(ctx, tx, target.hostUUIDs, deleteCmd); err != nil {
 			return ctxerr.Wrap(ctx, err, "inserting delete commands for hosts")
 		}
 		enqueuedTargets[profUUID] = target
@@ -1278,18 +1342,23 @@ func (ds *Datastore) cancelWindowsHostInstallsForDeletedMDMProfiles(
 	// This covers both install rows (being flipped to remove) and remove+NULL rows
 	// (being given a command_uuid and set to pending).
 	for profUUID, target := range enqueuedTargets {
-		upStmt, upArgs, err := sqlx.In(
-			`UPDATE host_mdm_windows_profiles
-			SET operation_type = ?, status = ?, command_uuid = ?, detail = ''
-			WHERE profile_uuid = ? AND host_uuid IN (?)`,
-			fleet.MDMOperationTypeRemove, fleet.MDMDeliveryPending, target.cmdUUID,
-			profUUID, target.hostUUIDs,
-		)
-		if err != nil {
-			return ctxerr.Wrap(ctx, err, "building IN for phase 2 update")
-		}
-		if _, err := tx.ExecContext(ctx, upStmt, upArgs...); err != nil {
-			return ctxerr.Wrap(ctx, err, "updating host profiles to remove")
+		if err := common_mysql.BatchProcessSimple(target.hostUUIDs, windowsMDMProfileDeleteBatchSize, func(batch []string) error {
+			upStmt, upArgs, err := sqlx.In(
+				`UPDATE host_mdm_windows_profiles
+				SET operation_type = ?, status = ?, command_uuid = ?, detail = ''
+				WHERE profile_uuid = ? AND host_uuid IN (?)`,
+				fleet.MDMOperationTypeRemove, fleet.MDMDeliveryPending, target.cmdUUID,
+				profUUID, batch,
+			)
+			if err != nil {
+				return ctxerr.Wrap(ctx, err, "building IN for phase 2 update")
+			}
+			if _, err := tx.ExecContext(ctx, upStmt, upArgs...); err != nil {
+				return ctxerr.Wrap(ctx, err, "updating host profiles to remove")
+			}
+			return nil
+		}); err != nil {
+			return err
 		}
 	}
 
@@ -2560,6 +2629,82 @@ ON DUPLICATE KEY UPDATE
 		}
 	}
 
+	// For profiles being updated (same name, different content), diff the old
+	// and new LocURIs. Generate <Delete> commands for LocURIs that were removed
+	// so the device reverts those settings.
+	//
+	// This is an edge case (most edits change values, not remove LocURIs).
+	// The delete commands are best-effort and currently not visible to the
+	// IT admin in the UI or API. They are fire-and-forget MDM commands
+	// with no corresponding host_mdm_windows_profiles status entry.
+	// Collect all LocURIs across incoming profiles AND reserved profiles that
+	// are kept even when not in the incoming list (e.g. "Windows OS Updates").
+	// This prevents deleting LocURIs that are still enforced by any profile
+	// that will remain after the batch-set.
+	allRetainedURIs := make(map[string]bool)
+	for _, p := range incomingProfs {
+		for _, uri := range fleet.ExtractLocURIsFromProfileBytes(p.SyncML) {
+			allRetainedURIs[uri] = true
+		}
+	}
+	// Include LocURIs from reserved profiles that are always kept.
+	for _, ep := range existingProfiles {
+		if _, isReserved := mdm.FleetReservedProfileNames()[ep.Name]; isReserved {
+			for _, uri := range fleet.ExtractLocURIsFromProfileBytes(ep.SyncML) {
+				allRetainedURIs[uri] = true
+			}
+		}
+	}
+
+	for _, existing := range existingProfiles {
+		incoming := incomingProfs[existing.Name]
+		if incoming == nil || bytes.Equal(existing.SyncML, incoming.SyncML) {
+			continue
+		}
+
+		oldURIs := fleet.ExtractLocURIsFromProfileBytes(existing.SyncML)
+		newURIs := fleet.ExtractLocURIsFromProfileBytes(incoming.SyncML)
+
+		newSet := make(map[string]bool, len(newURIs))
+		for _, u := range newURIs {
+			newSet[u] = true
+		}
+
+		var removedURIs []string
+		for _, u := range oldURIs {
+			// Skip if the LocURI is still in the updated version of this profile,
+			// or if another profile in the batch still targets it.
+			if !newSet[u] && !allRetainedURIs[u] {
+				removedURIs = append(removedURIs, u)
+			}
+		}
+
+		if len(removedURIs) == 0 {
+			continue
+		}
+
+		cmdUUID := uuid.NewString()
+		deleteCmd, err := fleet.BuildDeleteCommandFromLocURIs(removedURIs, cmdUUID)
+		if err != nil || deleteCmd == nil {
+			continue
+		}
+
+		// Find hosts that have this profile installed (not pending removal).
+		var hostUUIDs []string
+		if err := sqlx.SelectContext(ctx, tx, &hostUUIDs,
+			`SELECT host_uuid FROM host_mdm_windows_profiles WHERE profile_uuid = ? AND operation_type = ? AND status IS NOT NULL`,
+			existing.ProfileUUID, fleet.MDMOperationTypeInstall); err != nil {
+			return false, ctxerr.Wrap(ctx, err, "selecting hosts for edited profile LocURI cleanup")
+		}
+		if len(hostUUIDs) > 0 {
+			ds.logger.InfoContext(ctx, "sending delete commands for LocURIs removed from edited profile",
+				"profile.name", existing.Name, "profile.uuid", existing.ProfileUUID, "removed_loc_uris", len(removedURIs))
+			if err := ds.mdmWindowsInsertCommandForHostUUIDsDB(ctx, tx, hostUUIDs, deleteCmd); err != nil {
+				return false, ctxerr.Wrap(ctx, err, "inserting delete commands for removed LocURIs")
+			}
+		}
+	}
+
 	// insert the new profiles and the ones that have changed
 	for _, p := range incomingProfs {
 		if result, err = tx.ExecContext(ctx, insertNewOrEditedProfile, profTeamID, p.Name,
diff --git a/server/fleet/microsoft_mdm.go b/server/fleet/microsoft_mdm.go
index 4f400e401b..6bf002266a 100644
--- a/server/fleet/microsoft_mdm.go
+++ b/server/fleet/microsoft_mdm.go
@@ -1754,90 +1754,49 @@ func BuildDeleteCommandFromProfileBytes(profileBytes []byte, commandUUID string,
 		normalized = fmt.Appendf([]byte{}, "<Atomic>%s</Atomic>", normalized)
 	}
 
-	cmds, err := UnmarshallMultiTopLevelXMLProfile(normalized)
-	if err != nil {
-		return nil, fmt.Errorf("unmarshalling profile bytes for delete: %w", err)
-	}
-	if len(cmds) == 0 {
-		return nil, errors.New("no commands found in profile")
+	allURIs := ExtractLocURIsFromProfileBytes(normalized)
+	if len(allURIs) == 0 {
+		return nil, nil
 	}
 
-	// extractLocURIs collects all Target LocURIs from Replace and Add commands. Exec commands are intentionally excluded.
-	extractLocURIs := func(cmd *SyncMLCmd) []string {
-		var uris []string
-		for _, nested := range cmd.ReplaceCommands {
-			if uri := nested.GetTargetURI(); uri != "" {
-				uris = append(uris, uri)
-			}
-		}
-		for _, nested := range cmd.AddCommands {
-			if uri := nested.GetTargetURI(); uri != "" {
-				uris = append(uris, uri)
-			}
-		}
-		return uris
-	}
-
-	// makeDeleteCmd creates a single <Delete> SyncMLCmd for the given LocURI.
-	makeDeleteCmd := func(locURI string, cmdID string) SyncMLCmd {
-		target := locURI
-		return SyncMLCmd{
-			XMLName: xml.Name{Local: CmdDelete},
-			CmdID:   CmdID{Value: cmdID, IncludeFleetComment: true},
-			Items:   []CmdItem{{Target: &target}},
-		}
-	}
-
-	// Build the set of protected LocURIs from the variadic parameter.
+	// Filter out LocURIs that are still targeted by other active profiles.
 	inUse := make(map[string]bool)
 	if len(locURIsInUseByOtherProfiles) > 0 && locURIsInUseByOtherProfiles[0] != nil {
 		inUse = locURIsInUseByOtherProfiles[0]
 	}
 
-	// safeToDelete returns true if the LocURI is safe to delete (no other
-	// active profile targets it).
-	safeToDelete := func(uri string) bool {
-		return !inUse[uri]
-	}
-
-	var rawCommand []byte
-
-	// Collect all LocURIs to delete. For Atomic profiles, extract from nested
-	// commands; for non-atomic, extract from top-level commands.
-	var allURIs []string
-	switch {
-	case len(cmds) == 1 && cmds[0].XMLName.Local == CmdAtomic:
-		allURIs = extractLocURIs(&cmds[0])
-	default:
-		for _, cmd := range cmds {
-			if cmd.XMLName.Local == CmdExec {
-				continue
-			}
-			if uri := cmd.GetTargetURI(); uri != "" {
-				allURIs = append(allURIs, uri)
-			}
-		}
-	}
-
-	// Filter out protected URIs and build individual <Delete> commands.
-	// Never wrap in <Atomic> — removal is best-effort, and <Atomic> would
-	// cause all deletes to roll back (507) if any single one fails.
-	var deleteCmds []SyncMLCmd
+	var safeURIs []string
 	for _, uri := range allURIs {
-		if !safeToDelete(uri) {
-			continue
+		if !inUse[uri] {
+			safeURIs = append(safeURIs, uri)
 		}
+	}
+
+	return BuildDeleteCommandFromLocURIs(safeURIs, commandUUID)
+}
+
+// BuildDeleteCommandFromLocURIs generates individual <Delete> commands for
+// the given LocURIs. Returns nil if locURIs is empty.
+func BuildDeleteCommandFromLocURIs(locURIs []string, commandUUID string) (*MDMWindowsCommand, error) {
+	if len(locURIs) == 0 {
+		return nil, nil
+	}
+
+	var deleteCmds []SyncMLCmd
+	for _, uri := range locURIs {
 		cmdID := uuid.NewString()
 		if len(deleteCmds) == 0 {
 			cmdID = commandUUID
 		}
-		deleteCmds = append(deleteCmds, makeDeleteCmd(uri, cmdID))
-	}
-	if len(deleteCmds) == 0 {
-		return nil, nil
+		target := uri
+		deleteCmds = append(deleteCmds, SyncMLCmd{
+			XMLName: xml.Name{Local: CmdDelete},
+			CmdID:   CmdID{Value: cmdID, IncludeFleetComment: true},
+			Items:   []CmdItem{{Target: &target}},
+		})
 	}
 
-	rawCommand, err = xml.Marshal(deleteCmds)
+	rawCommand, err := xml.Marshal(deleteCmds)
 	if err != nil {
 		return nil, fmt.Errorf("marshalling delete commands: %w", err)
 	}
@@ -1870,3 +1829,41 @@ func UnmarshallMultiTopLevelXMLProfile(profileBytes []byte) ([]SyncMLCmd, error)
 
 	return root.Commands, nil
 }
+
+// ExtractLocURIsFromProfileBytes returns all Target LocURIs found in the
+// profile's Replace and Add commands. Exec commands are excluded (they
+// trigger one-time actions, not persistent settings). For Atomic profiles,
+// nested commands are inspected.
+func ExtractLocURIsFromProfileBytes(profileBytes []byte) []string {
+	// Mirror the install-side SCEP normalization.
+	normalized := profileBytes
+	if strings.Contains(string(normalized), WINDOWS_SCEP_LOC_URI_PART) && !strings.Contains(string(normalized), "<Atomic>") {
+		normalized = fmt.Appendf([]byte{}, "<Atomic>%s</Atomic>", normalized)
+	}
+
+	cmds, err := UnmarshallMultiTopLevelXMLProfile(normalized)
+	if err != nil || len(cmds) == 0 {
+		return nil
+	}
+
+	var uris []string
+	for _, cmd := range cmds {
+		if cmd.XMLName.Local == CmdAtomic {
+			for _, nested := range cmd.ReplaceCommands {
+				if uri := nested.GetTargetURI(); uri != "" {
+					uris = append(uris, uri)
+				}
+			}
+			for _, nested := range cmd.AddCommands {
+				if uri := nested.GetTargetURI(); uri != "" {
+					uris = append(uris, uri)
+				}
+			}
+		} else if cmd.XMLName.Local == CmdReplace || cmd.XMLName.Local == CmdAdd {
+			if uri := cmd.GetTargetURI(); uri != "" {
+				uris = append(uris, uri)
+			}
+		}
+	}
+	return uris
+}
diff --git a/server/fleet/microsoft_mdm_test.go b/server/fleet/microsoft_mdm_test.go
index e5c2b7cdf8..f84fb563e9 100644
--- a/server/fleet/microsoft_mdm_test.go
+++ b/server/fleet/microsoft_mdm_test.go
@@ -540,9 +540,9 @@ func TestBuildDeleteCommandFromProfileBytes(t *testing.T) {
 			expectNil: true,
 		},
 		{
-			name:        "empty profile",
-			profileXML:  "",
-			expectError: "no commands found in profile",
+			name:       "empty profile returns nil",
+			profileXML: "",
+			expectNil:  true,
 		},
 	}
 
@@ -780,3 +780,35 @@ func TestBuildMDMWindowsProfilePayloadFromMDMResponseRemoveOperation(t *testing.
 		require.Equal(t, MDMDeliveryVerified, *payload.Status)
 	})
 }
+
+func TestExtractLocURIsFromProfileBytes(t *testing.T) {
+	t.Parallel()
+	t.Run("atomic profile", func(t *testing.T) {
+		xml := `<Atomic><Replace><Item><Target><LocURI>./Device/A</LocURI></Target></Item></Replace><Replace><Item><Target><LocURI>./Device/B</LocURI></Target></Item></Replace></Atomic>`
+		uris := ExtractLocURIsFromProfileBytes([]byte(xml))
+		require.Equal(t, []string{"./Device/A", "./Device/B"}, uris)
+	})
+
+	t.Run("non-atomic profile", func(t *testing.T) {
+		xml := `<Replace><Item><Target><LocURI>./Device/X</LocURI></Target></Item></Replace><Replace><Item><Target><LocURI>./Device/Y</LocURI></Target></Item></Replace>`
+		uris := ExtractLocURIsFromProfileBytes([]byte(xml))
+		require.Equal(t, []string{"./Device/X", "./Device/Y"}, uris)
+	})
+
+	t.Run("exec commands excluded", func(t *testing.T) {
+		xml := `<Replace><Item><Target><LocURI>./Device/A</LocURI></Target></Item></Replace><Exec><Item><Target><LocURI>./Device/Enroll</LocURI></Target></Item></Exec>`
+		uris := ExtractLocURIsFromProfileBytes([]byte(xml))
+		require.Equal(t, []string{"./Device/A"}, uris)
+	})
+
+	t.Run("empty profile", func(t *testing.T) {
+		uris := ExtractLocURIsFromProfileBytes([]byte(""))
+		require.Nil(t, uris)
+	})
+
+	t.Run("delete commands excluded", func(t *testing.T) {
+		xml := `<Replace><Item><Target><LocURI>./Device/A</LocURI></Target></Item></Replace><Delete><Item><Target><LocURI>./Device/B</LocURI></Target></Item></Delete>`
+		uris := ExtractLocURIsFromProfileBytes([]byte(xml))
+		require.Equal(t, []string{"./Device/A"}, uris)
+	})
+}
diff --git a/server/service/integration_mdm_profiles_test.go b/server/service/integration_mdm_profiles_test.go
index 93aeb97028..70e7d498b6 100644
--- a/server/service/integration_mdm_profiles_test.go
+++ b/server/service/integration_mdm_profiles_test.go
@@ -4423,6 +4423,176 @@ func (s *integrationMDMTestSuite) TestWindowsProfileManagement() {
 	res = s.DoRaw("POST", fmt.Sprintf("/api/latest/fleet/hosts/%d/configuration_profiles/%s/resend", host.ID, mcUUID), nil, http.StatusUnprocessableEntity)
 	errMsg = extractServerErrorText(res.Body)
 	require.Contains(t, errMsg, "Profile is not compatible with host platform")
+
+	t.Run("edit_profile_removes_locuri_sends_delete", func(t *testing.T) {
+		// Editing a profile to remove a LocURI should send a <Delete> for the removed LocURI.
+		// Create a profile with two LocURIs via batch-set, then edit it to have only one.
+		// The device should receive a <Delete> for the removed LocURI plus an install for the updated profile.
+
+		// First, clean up: use batch-set with only our new test profile to remove all
+		// existing team profiles cleanly (this goes through the proper deletion path).
+		twoLocURIProfile := `<Atomic><Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Camera/AllowCamera</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace><Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Experience/AllowCortana</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace></Atomic>`
+		// Also disable OS updates to simplify
+		tmResp := teamResponse{}
+		s.DoJSON("PATCH", fmt.Sprintf("/api/latest/fleet/teams/%d", tm.ID), json.RawMessage(`{"mdm": { "windows_updates": {"deadline_days": null, "grace_period_days": null} }}`), http.StatusOK, &tmResp)
+		s.Do("POST", "/api/v1/fleet/mdm/profiles/batch",
+			batchSetMDMProfilesRequest{Profiles: []fleet.MDMProfileBatchPayload{
+				{Name: "edit-locuri-test", Contents: []byte(twoLocURIProfile)},
+			}}, http.StatusNoContent, "team_id", fmt.Sprint(tm.ID))
+
+		// Trigger profile sync: device gets the new profile + delete commands for old profiles.
+		// Drain all commands from the device without asserting exact counts (cleanup varies).
+		s.awaitTriggerProfileSchedule(t)
+		cmds, err := mdmDevice.StartManagementSession()
+		require.NoError(t, err)
+		msgID, err := mdmDevice.GetCurrentMsgID()
+		require.NoError(t, err)
+		for _, c := range cmds {
+			cmdID := c.Cmd.CmdID
+			status := syncml.CmdStatusOK
+			mdmDevice.AppendResponse(fleet.SyncMLCmd{
+				XMLName: xml.Name{Local: fleet.CmdStatus},
+				MsgRef:  &msgID,
+				CmdRef:  &cmdID.Value,
+				Cmd:     ptr.String(c.Verb),
+				Data:    &status,
+				CmdID:   fleet.CmdID{Value: uuid.NewString()},
+			})
+		}
+		_, err = mdmDevice.SendResponse()
+		require.NoError(t, err)
+
+		// Drain any remaining commands until the device is clean.
+		verifyProfiles(mdmDevice, 0, false)
+
+		// Now edit the profile to remove AllowCortana, keeping only AllowCamera.
+		oneLocURIProfile := `<Atomic><Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Camera/AllowCamera</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace></Atomic>`
+		s.Do("POST", "/api/v1/fleet/mdm/profiles/batch",
+			batchSetMDMProfilesRequest{Profiles: []fleet.MDMProfileBatchPayload{
+				{Name: "edit-locuri-test", Contents: []byte(oneLocURIProfile)},
+			}}, http.StatusNoContent, "team_id", fmt.Sprint(tm.ID))
+
+		// Trigger profile sync: device should get:
+		// - 1 <Delete> for the removed AllowCortana LocURI (from batchSet edit diff)
+		// - 1 Atomic install for the updated profile (from reconciler checksum mismatch)
+		// Total: 2 Status + 1 Delete + 1 Atomic = 4 commands
+		s.awaitTriggerProfileSchedule(t)
+		cmds, err = mdmDevice.StartManagementSession()
+		require.NoError(t, err)
+		require.Len(t, cmds, 4, "expected 2 status + 1 delete + 1 install")
+
+		var gotDelete, gotInstall bool
+		msgID, err = mdmDevice.GetCurrentMsgID()
+		require.NoError(t, err)
+		for _, c := range cmds {
+			cmdID := c.Cmd.CmdID
+			status := syncml.CmdStatusOK
+			switch c.Verb {
+			case "Delete":
+				gotDelete = true
+				require.Contains(t, c.Cmd.GetTargetURI(), "AllowCortana",
+					"Delete should target the removed LocURI")
+			case "Atomic":
+				if len(c.Cmd.ReplaceCommands) > 0 {
+					gotInstall = true
+					// Verify the install only has AllowCamera, not AllowCortana
+					var installURIs []string
+					for _, rc := range c.Cmd.ReplaceCommands {
+						installURIs = append(installURIs, rc.GetTargetURI())
+					}
+					require.Len(t, installURIs, 1)
+					require.Contains(t, installURIs[0], "AllowCamera")
+				}
+			}
+			mdmDevice.AppendResponse(fleet.SyncMLCmd{
+				XMLName: xml.Name{Local: fleet.CmdStatus},
+				MsgRef:  &msgID,
+				CmdRef:  &cmdID.Value,
+				Cmd:     ptr.String(c.Verb),
+				Data:    &status,
+				Items:   nil,
+				CmdID:   fleet.CmdID{Value: uuid.NewString()},
+			})
+		}
+		require.True(t, gotDelete, "expected a Delete command for the removed LocURI")
+		require.True(t, gotInstall, "expected an install command for the updated profile")
+
+		cmds, err = mdmDevice.SendResponse()
+		require.NoError(t, err)
+		require.Len(t, cmds, 1) // just the ack
+	})
+
+	t.Run("edit_profile_does_not_delete_locuri_used_by_another_profile", func(t *testing.T) {
+		// If profile A has LocURIs X, Y and profile B has LocURI Y,
+		// editing A to remove Y should NOT send a <Delete> for Y
+		// because profile B still enforces it.
+
+		// Set up two profiles that share a LocURI (AllowCamera).
+		profileA := `<Atomic><Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Camera/AllowCamera</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace><Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Experience/AllowCortana</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace></Atomic>`
+		profileB := `<Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Camera/AllowCamera</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>1</Data></Item></Replace>`
+		s.Do("POST", "/api/v1/fleet/mdm/profiles/batch",
+			batchSetMDMProfilesRequest{Profiles: []fleet.MDMProfileBatchPayload{
+				{Name: "shared-locuri-A", Contents: []byte(profileA)},
+				{Name: "shared-locuri-B", Contents: []byte(profileB)},
+			}}, http.StatusNoContent, "team_id", fmt.Sprint(tm.ID))
+
+		// Drain install commands.
+		s.awaitTriggerProfileSchedule(t)
+		cmds, err := mdmDevice.StartManagementSession()
+		require.NoError(t, err)
+		msgID, err := mdmDevice.GetCurrentMsgID()
+		require.NoError(t, err)
+		for _, c := range cmds {
+			cmdID := c.Cmd.CmdID
+			status := syncml.CmdStatusOK
+			mdmDevice.AppendResponse(fleet.SyncMLCmd{
+				XMLName: xml.Name{Local: fleet.CmdStatus},
+				MsgRef:  &msgID,
+				CmdRef:  &cmdID.Value,
+				Cmd:     ptr.String(c.Verb),
+				Data:    &status,
+				CmdID:   fleet.CmdID{Value: uuid.NewString()},
+			})
+		}
+		_, err = mdmDevice.SendResponse()
+		require.NoError(t, err)
+		verifyProfiles(mdmDevice, 0, false)
+
+		// Edit profile A to remove AllowCamera (shared with B), keep only AllowCortana.
+		profileAEdited := `<Replace><Item><Target><LocURI>./Device/Vendor/MSFT/Policy/Config/Experience/AllowCortana</LocURI></Target><Meta><Format xmlns="syncml:metinf">int</Format></Meta><Data>0</Data></Item></Replace>`
+		s.Do("POST", "/api/v1/fleet/mdm/profiles/batch",
+			batchSetMDMProfilesRequest{Profiles: []fleet.MDMProfileBatchPayload{
+				{Name: "shared-locuri-A", Contents: []byte(profileAEdited)},
+				{Name: "shared-locuri-B", Contents: []byte(profileB)},
+			}}, http.StatusNoContent, "team_id", fmt.Sprint(tm.ID))
+
+		// Trigger sync: should get an install for the updated A, but NO delete
+		// for AllowCamera since profile B still uses it.
+		s.awaitTriggerProfileSchedule(t)
+		cmds, err = mdmDevice.StartManagementSession()
+		require.NoError(t, err)
+
+		msgID, err = mdmDevice.GetCurrentMsgID()
+		require.NoError(t, err)
+		for _, c := range cmds {
+			if c.Verb == "Delete" {
+				require.NotContains(t, c.Cmd.GetTargetURI(), "AllowCamera",
+					"should NOT delete AllowCamera because profile B still uses it")
+			}
+			cmdID := c.Cmd.CmdID
+			status := syncml.CmdStatusOK
+			mdmDevice.AppendResponse(fleet.SyncMLCmd{
+				XMLName: xml.Name{Local: fleet.CmdStatus},
+				MsgRef:  &msgID,
+				CmdRef:  &cmdID.Value,
+				Cmd:     ptr.String(c.Verb),
+				Data:    &status,
+				CmdID:   fleet.CmdID{Value: uuid.NewString()},
+			})
+		}
+		_, err = mdmDevice.SendResponse()
+		require.NoError(t, err)
+	})
 }
 
 func (s *integrationMDMTestSuite) TestApplyTeamsMDMWindowsProfiles() {
diff --git a/server/service/microsoft_mdm.go b/server/service/microsoft_mdm.go
index 72dc03925a..ac855120a7 100644
--- a/server/service/microsoft_mdm.go
+++ b/server/service/microsoft_mdm.go
@@ -2754,14 +2754,8 @@ func ReconcileWindowsProfiles(ctx context.Context, ds fleet.Datastore, logger *s
 			if _, isBeingRemoved := removeTargets[otherUUID]; isBeingRemoved {
 				continue // also being removed, don't protect its URIs
 			}
-			otherCmds, err := fleet.UnmarshallMultiTopLevelXMLProfile(otherContent.SyncML)
-			if err != nil {
-				continue
-			}
-			for _, cmd := range otherCmds {
-				if uri := cmd.GetTargetURI(); uri != "" {
-					activeLocURIs[uri] = true
-				}
+			for _, uri := range fleet.ExtractLocURIsFromProfileBytes(otherContent.SyncML) {
+				activeLocURIs[uri] = true
 			}
 		}