diff --git a/src/resolve/resolved-dns-dnssec.c b/src/resolve/resolved-dns-dnssec.c
index d987ee4fa4..36eb3595d5 100644
--- a/src/resolve/resolved-dns-dnssec.c
+++ b/src/resolve/resolved-dns-dnssec.c
@@ -12,7 +12,6 @@
 #include "memory-util.h"
 #include "memstream-util.h"
 #include "resolved-dns-dnssec.h"
-#include "resolved-util.h"
 #include "sort-util.h"
 #include "string-table.h"
 #include "string-util.h"
@@ -717,7 +716,7 @@ int dnssec_verify_rrset(
         assert(dnskey);
         assert(result);
 
-        r = DLOPEN_LIBCRYPTO(LOG_DEBUG, DLOPEN_LIBCRYPTO_PRIORITY);
+        r = DLOPEN_LIBCRYPTO(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED);
         if (r < 0)
                 return r;
 
@@ -1074,7 +1073,7 @@ int dnssec_verify_dnskey_by_ds(DnsResourceRecord *dnskey, DnsResourceRecord *ds,
         assert(dnskey);
         assert(ds);
 
-        r = DLOPEN_LIBCRYPTO(LOG_DEBUG, DLOPEN_LIBCRYPTO_PRIORITY);
+        r = DLOPEN_LIBCRYPTO(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED);
         if (r < 0)
                 return r;
 
@@ -1214,7 +1213,7 @@ int dnssec_nsec3_hash(DnsResourceRecord *nsec3, const char *name, void *ret) {
         assert(name);
         assert(ret);
 
-        r = DLOPEN_LIBCRYPTO(LOG_DEBUG, DLOPEN_LIBCRYPTO_PRIORITY);
+        r = DLOPEN_LIBCRYPTO(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED);
         if (r < 0)
                 return r;
 
diff --git a/src/resolve/resolved-dns-transaction.c b/src/resolve/resolved-dns-transaction.c
index a14aa0de7d..4268cd3ff0 100644
--- a/src/resolve/resolved-dns-transaction.c
+++ b/src/resolve/resolved-dns-transaction.c
@@ -786,8 +786,20 @@ static int dns_transaction_emit_tcp(DnsTransaction *t) {
 
                         assert(t->server);
                         r = dnstls_stream_connect_tls(s, t->server);
-                        if (r < 0)
+                        if (r < 0) {
+                                /* If libcrypto is not available treat this like a TLS connection loss, so
+                                 * that opportunistic DNS-over-TLS downgrades to plaintext instead of
+                                 * re-selecting a TLS feature level and failing on every attempt. */
+                                if (r == -EOPNOTSUPP) {
+                                        log_struct_once(LOG_WARNING,
+                                                        LOG_MESSAGE_ID(SD_MESSAGE_MISSING_DEPENDENCY_STR),
+                                                        LOG_ITEM("FEATURE=DNS-over-TLS"),
+                                                        LOG_MESSAGE("DNS-over-TLS has been requested but the required TLS libraries (libssl/libcrypto) are not installed."));
+                                        dns_server_packet_lost(t->server, IPPROTO_TCP, t->current_feature_level);
+                                        return -ECONNREFUSED;
+                                }
                                 return r;
+                        }
                 }
 #endif
 
diff --git a/src/resolve/resolved-dnstls.c b/src/resolve/resolved-dnstls.c
index 6f489ae3bd..6bcbdb5260 100644
--- a/src/resolve/resolved-dnstls.c
+++ b/src/resolve/resolved-dnstls.c
@@ -71,6 +71,10 @@ int dnstls_stream_connect_tls(DnsStream *stream, DnsServer *server) {
         assert(stream->manager);
         assert(server);
 
+        r = dnstls_manager_init(stream->manager);
+        if (r < 0)
+                return r;
+
         rb = sym_BIO_new_socket(stream->fd, 0);
         if (!rb)
                 return -ENOMEM;
@@ -398,31 +402,39 @@ void dnstls_server_free(DnsServer *server) {
 }
 
 int dnstls_manager_init(Manager *manager) {
+        _cleanup_(SSL_CTX_freep) SSL_CTX *ctx = NULL;
         int r;
 
         assert(manager);
 
-        r = DLOPEN_LIBCRYPTO(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_REQUIRED);
+        /* Load libcrypto/libssl on first use, so that the dependencies can be optional. */
+
+        if (manager->dnstls_data.ctx)
+                return 0;
+
+        r = DLOPEN_LIBCRYPTO(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED);
         if (r < 0)
                 return r;
 
-        r = DLOPEN_LIBSSL(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_REQUIRED);
+        r = DLOPEN_LIBSSL(LOG_WARNING, SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED);
         if (r < 0)
                 return r;
 
-        manager->dnstls_data.ctx = sym_SSL_CTX_new(sym_TLS_client_method());
-        if (!manager->dnstls_data.ctx)
+        ctx = sym_SSL_CTX_new(sym_TLS_client_method());
+        if (!ctx)
                 return log_openssl_errors(LOG_WARNING, "Failed to create SSL context");
 
-        r = sym_SSL_CTX_set_min_proto_version(manager->dnstls_data.ctx, TLS1_2_VERSION);
+        r = sym_SSL_CTX_set_min_proto_version(ctx, TLS1_2_VERSION);
         if (r == 0)
                 return log_openssl_errors(LOG_WARNING, "Failed to set protocol version on SSL context");
 
-        (void) sym_SSL_CTX_set_options(manager->dnstls_data.ctx, SSL_OP_NO_COMPRESSION);
+        (void) sym_SSL_CTX_set_options(ctx, SSL_OP_NO_COMPRESSION);
 
-        r = sym_SSL_CTX_set_default_verify_paths(manager->dnstls_data.ctx);
+        r = sym_SSL_CTX_set_default_verify_paths(ctx);
         if (r == 0)
                 return log_openssl_errors(LOG_WARNING, "Failed to load system trust store");
+
+        manager->dnstls_data.ctx = TAKE_PTR(ctx);
         return 0;
 }
 
diff --git a/src/resolve/resolved-manager.c b/src/resolve/resolved-manager.c
index 29a7046be3..faf539195b 100644
--- a/src/resolve/resolved-manager.c
+++ b/src/resolve/resolved-manager.c
@@ -754,12 +754,6 @@ int manager_new(Manager **ret) {
         if (r < 0)
                 log_warning_errno(r, "Failed to parse configuration file, ignoring: %m");
 
-#if ENABLE_DNS_OVER_TLS
-        r = dnstls_manager_init(m);
-        if (r < 0)
-                return r;
-#endif
-
         r = sd_event_default(&m->event);
         if (r < 0)
                 return r;
diff --git a/src/resolve/resolved-util.h b/src/resolve/resolved-util.h
index 9e84b44145..446b7c9f1b 100644
--- a/src/resolve/resolved-util.h
+++ b/src/resolve/resolved-util.h
@@ -1,12 +1,4 @@
 /* SPDX-License-Identifier: LGPL-2.1-or-later */
 #pragma once
 
-#include "sd-dlopen.h"
-
-#if ENABLE_DNS_OVER_TLS
-#  define DLOPEN_LIBCRYPTO_PRIORITY SD_ELF_NOTE_DLOPEN_PRIORITY_REQUIRED
-#else
-#  define DLOPEN_LIBCRYPTO_PRIORITY SD_ELF_NOTE_DLOPEN_PRIORITY_RECOMMENDED
-#endif
-
 int resolve_system_hostname(char **full_hostname, char **first_label);